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Annual Review of Microbiology

Volume 71, 2017

Evolutionary Genomics of Defense Systems in Archaea and Bacteria*

Abstract

Evolution of bacteria and archaea involves an incessant arms race against an enormous diversity of genetic parasites. Accordingly, a substantial fraction of the genes in most bacteria and archaea are dedicated to antiparasite defense. The functions of these defense systems follow several distinct strategies, including innate immunity; adaptive immunity; and dormancy induction, or programmed cell death. Recent comparative genomic studies taking advantage of the expanding database of microbial genomes and metagenomes, combined with direct experiments, resulted in the discovery of several previously unknown defense systems, including innate immunity centered on Argonaute proteins, bacteriophage exclusion, and new types of CRISPR-Cas systems of adaptive immunity. Some general principles of function and evolution of defense systems are starting to crystallize, in particular, extensive gain and loss of defense genes during the evolution of prokaryotes; formation of genomic defense islands; evolutionary connections between mobile genetic elements and defense, whereby genes of mobile elements are repeatedly recruited for defense functions; the partially selfish and addictive behavior of the defense systems; and coupling between immunity and dormancy induction/programmed cell death.

Keyword(s): adaptive immunity, antivirus defense, CRISPR-Cas, dormancy, innate immunity, mobile genetic elements, programmed cell death, restriction-modification, toxins-antitoxins
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/content/journals/10.1146/annurev-micro-090816-093830
2017-09-08
2024-04-16
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Literature Cited

  1. Abudayyeh OO, Gootenberg JS, Konermann S, Joung J, Slaymaker IM. 1.  et al. 2016. C2c2 is a single-component programmable RNA-guided RNA-targeting CRISPR effector. Science 353:aaf5573 [Google Scholar]
  2. Amitai G, Sorek R. 2.  2016. CRISPR-Cas adaptation: insights into the mechanism of action. Nat. Rev. Microbiol. 14:67–76 [Google Scholar]
  3. Anantharaman V, Makarova KS, Burroughs AM, Koonin EV, Aravind L. 3.  2013. Comprehensive analysis of the HEPN superfamily: identification of novel roles in intra-genomic conflicts, defense, pathogenesis and RNA processing. Biol. Direct 8:15 [Google Scholar]
  4. Aravind L, Koonin EV. 4.  1999. DNA polymerase beta-like nucleotidyltransferase superfamily: identification of three new families, classification and evolutionary history. Nucleic Acids Res 27:1609–18 [Google Scholar]
  5. Aravind L, Watanabe H, Lipman DJ, Koonin EV. 5.  2000. Lineage-specific loss and divergence of functionally linked genes in eukaryotes. PNAS 97:11319–24 [Google Scholar]
  6. Aziz RK, Breitbart M, Edwards RA. 6.  2010. Transposases are the most abundant, most ubiquitous genes in nature. Nucleic Acids Res 38:4207–17 [Google Scholar]
  7. Barrangou R. 7.  2013. CRISPR-Cas systems and RNA-guided interference. Wiley Interdiscip. Rev. RNA 4:267–78 [Google Scholar]
  8. Barrangou R, van der Oost J. 8.  2015. Bacteriophage exclusion, a new defense system. EMBO J 34:134–35 [Google Scholar]
  9. Beguin P, Charpin N, Koonin EV, Forterre P, Krupovic M. 9.  2016. Casposon integration shows strong target site preference and recapitulates protospacer integration by CRISPR-Cas systems. Nucleic Acids Res 44:10367–76 [Google Scholar]
  10. Beloglazova N, Brown G, Zimmerman MD, Proudfoot M, Makarova KS. 10.  et al. 2008. A novel family of sequence-specific endoribonucleases associated with the clustered regularly interspaced short palindromic repeats. J. Biol. Chem. 283:20361–71 [Google Scholar]
  11. Bhaya D, Davison M, Barrangou R. 11.  2011. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu. Rev. Genet. 45:273–97 [Google Scholar]
  12. Bikard D, Marraffini LA. 12.  2012. Innate and adaptive immunity in bacteria: mechanisms of programmed genetic variation to fight bacteriophages. Curr. Opin. Immunol. 24:15–20 [Google Scholar]
  13. Blanga-Kanfi S, Amitsur M, Azem A, Kaufmann G. 13.  2006. PrrC-anticodon nuclease: functional organization of a prototypical bacterial restriction RNase. Nucleic Acids Res 34:3209–19 [Google Scholar]
  14. Bohmert K, Camus I, Bellini C, Bouchez D, Caboche M, Benning C. 14.  1998. AGO1 defines a novel locus of Arabidopsis controlling leaf development. EMBO J 17:170–80 [Google Scholar]
  15. Bourniquel AA, Bickle TA. 15.  2002. Complex restriction enzymes: NTP-driven molecular motors. Biochimie 84:1047–59 [Google Scholar]
  16. Brantl S, Jahn N. 16.  2015. sRNAs in bacterial type I and type III toxin-antitoxin systems. FEMS Microbiol. Rev. 39:413–27 [Google Scholar]
  17. Brown CT, Hug LA, Thomas BC, Sharon I, Castelle CJ. 17.  et al. 2015. Unusual biology across a group comprising more than 15% of domain Bacteria. Nature 523:208–11 [Google Scholar]
  18. Burstein D, Sun CL, Brown CT, Sharon I, Anantharaman K. 18.  et al. 2016. Major bacterial lineages are essentially devoid of CRISPR-Cas viral defence systems. Nat. Commun. 7:10613 [Google Scholar]
  19. Butterer A, Pernstich C, Smith RM, Sobott F, Szczelkun MD, Toth J. 19.  2014. Type III restriction endonucleases are heterotrimeric: comprising one helicase-nuclease subunit and a dimeric methyltransferase that binds only one specific DNA. Nucleic Acids Res 42:5139–50 [Google Scholar]
  20. Carroll D. 20.  2012. A CRISPR approach to gene targeting. Mol. Ther. 20:1658–60 [Google Scholar]
  21. Cerutti H, Casas-Mollano JA. 21.  2006. On the origin and functions of RNA-mediated silencing: From protists to man. Curr. Genet. 50:81–99 [Google Scholar]
  22. Cerutti L, Mian N, Bateman A. 22.  2000. Domains in gene silencing and cell differentiation proteins: the novel PAZ domain and redefinition of the Piwi domain. Trends Biochem. Sci. 25:481–82 [Google Scholar]
  23. Chan WT, Espinosa M, Yeo CC. 23.  2016. Keeping the wolves at bay: antitoxins of prokaryotic type II toxin-antitoxin systems. Front. Mol. Biosci. 3:9 [Google Scholar]
  24. Charpentier E, Richter H, van der Oost J, White MF. 24.  2015. Biogenesis pathways of RNA guides in archaeal and bacterial CRISPR-Cas adaptive immunity. FEMS Microbiol. Rev. 39:428–41 [Google Scholar]
  25. Chaturongakul S, Ounjai P. 25.  2014. Phage-host interplay: examples from tailed phages and gram-negative bacterial pathogens. Front. Microbiol. 5:442 [Google Scholar]
  26. Chen F, Zhang Z, Lin K, Qian T, Zhang Y. 26.  et al. 2012. Crystal structure of the cysteine desulfurase DndA from Streptomyces lividans which is involved in DNA phosphorothioation. PLOS ONE 7:e36635 [Google Scholar]
  27. Chinenova TA, Mkrtumian NM, Lomovskaia ND. 27.  1982. [Genetic characteristics of a new phage resistance trait in Streptomyces coelicolor A3(2)]. In Russian. Genetika 18:1945–52 [Google Scholar]
  28. Chopin MC, Chopin A, Bidnenko E. 28.  2005. Phage abortive infection in lactococci: variations on a theme. Curr. Opin. Microbiol. 8:473–79 [Google Scholar]
  29. Christensen-Dalsgaard M, Overgaard M, Winther KS, Gerdes K. 29.  2008. RNA decay by messenger RNA interferases. Methods Enzymol 447:521–35 [Google Scholar]
  30. Dao-Thi MH, Van Melderen L, De Genst E, Afif H, Buts L. 30.  et al. 2005. Molecular basis of gyrase poisoning by the addiction toxin CcdB. J. Mol. Biol. 348:1091–102 [Google Scholar]
  31. Daume M, Plagens A, Randau L. 31.  2014. DNA binding properties of the small Cascade subunit Csa5. PLOS ONE 9:e105716 [Google Scholar]
  32. Dixit B, Ghosh KK, Fernandes G, Kumar P, Gogoi P, Kumar M. 32.  2016. Dual nuclease activity of a Cas2 protein in CRISPR-Cas subtype I-B of Leptospira interrogans. FEBS Lett. 590:1002–16 [Google Scholar]
  33. Domingues S, McGovern S, Plochocka D, Santos MA, Ehrlich SD. 33.  et al. 2008. The lactococcal abortive infection protein AbiP is membrane-anchored and binds nucleic acids. Virology 373:14–24 [Google Scholar]
  34. Dong D, Ren K, Qiu X, Zheng J, Guo M. 34.  et al. 2016. The crystal structure of Cpf1 in complex with CRISPR RNA. Nature 532:522–26 [Google Scholar]
  35. Durand S, Jahn N, Condon C, Brantl S. 35.  2012. Type I toxin-antitoxin systems in Bacillus subtilis. RNA Biol. 9:1491–97 [Google Scholar]
  36. Durmaz E, Klaenhammer TR. 36.  2007. Abortive phage resistance mechanism AbiZ speeds the lysis clock to cause premature lysis of phage-infected Lactococcus lactis. J. Bacteriol. 189:1417–25 [Google Scholar]
  37. East-Seletsky A, O'Connell MR, Knight SC, Burstein D, Cate JH. 37.  et al. 2016. Two distinct RNase activities of CRISPR-C2c2 enable guide-RNA processing and RNA detection. Nature 538:270–73 [Google Scholar]
  38. Eckstein F. 38.  2007. Phosphorothioation of DNA in bacteria. Nat. Chem. Biol. 3:689–90 [Google Scholar]
  39. Elmore JR, Sheppard NF, Ramia N, Deighan T, Li H. 39.  et al. 2016. Bipartite recognition of target RNAs activates DNA cleavage by the Type III-B CRISPR-Cas system. Genes Dev 30:447–59 [Google Scholar]
  40. Ershova AS, Karyagina AS, Vasiliev MO, Lyashchuk AM, Lunin VG. 40.  et al. 2012. Solitary restriction endonucleases in prokaryotic genomes. Nucleic Acids Res 40:10107–15 [Google Scholar]
  41. Ershova AS, Rusinov IS, Spirin SA, Karyagina AS, Alexeevski AV. 41.  2015. Role of restriction-modification systems in prokaryotic evolution and ecology. Biochemistry 80:1373–86 [Google Scholar]
  42. Fabre L, Zhang J, Guigon G, Le Hello S, Guibert V. 42.  et al. 2012. CRISPR typing and subtyping for improved laboratory surveillance of Salmonella infections. PLOS ONE 7:e36995 [Google Scholar]
  43. Fineran PC, Charpentier E. 43.  2012. Memory of viral infections by CRISPR-Cas adaptive immune systems: acquisition of new information. Virology 434:202–9 [Google Scholar]
  44. Fonfara I, Richter H, Bratovic M, Le Rhun A, Charpentier E. 44.  2016. The CRISPR-associated DNA-cleaving enzyme Cpf1 also processes precursor CRISPR RNA. Nature 532:517–21 [Google Scholar]
  45. Forterre P, Prangishvili D. 45.  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 [Google Scholar]
  46. Fozo EM, Hemm MR, Storz G. 46.  2008. Small toxic proteins and the antisense RNAs that repress them. Microbiol. Mol. Biol. Rev. 72:579–89 [Google Scholar]
  47. Frost LS, Leplae R, Summers AO, Toussaint A. 47.  2005. Mobile genetic elements: the agents of open source evolution. Nat. Rev. Microbiol. 3:722–32 [Google Scholar]
  48. Gelfand MS, Koonin EV. 48.  1997. Avoidance of palindromic words in bacterial and archaeal genomes: a close connection with restriction enzymes. Nucleic Acids Res 25:2430–39 [Google Scholar]
  49. Gerdes K. 49.  2012. Prokaryotic Toxin-Antitoxins Berlin: Springer
  50. Gerdes K, Christensen SK, Lobner-Olesen A. 50.  2005. Prokaryotic toxin-antitoxin stress response loci. Nat. Rev. Microbiol. 3:371–82 [Google Scholar]
  51. Goeders N, Van Melderen L. 51.  2014. Toxin-antitoxin systems as multilevel interaction systems. Toxins 6:304–24 [Google Scholar]
  52. Goldfarb T, Sberro H, Weinstock E, Cohen O, Doron S. 52.  et al. 2015. BREX is a novel phage resistance system widespread in microbial genomes. EMBO J 34:169–83 [Google Scholar]
  53. Gunderson FF, Mallama CA, Fairbairn SG, Cianciotto NP. 53.  2015. Nuclease activity of Legionella pneumophila Cas2 promotes intracellular infection of amoebal host cells. Infect. Immun. 83:1008–18 [Google Scholar]
  54. Haft DH, Selengut J, Mongodin EF, Nelson KE. 54.  2005. A guild of 45 CRISPR-associated (Cas) protein families and multiple CRISPR/Cas subtypes exist in prokaryotic genomes. PLOS Comput. Biol. 1:e60 [Google Scholar]
  55. Hayes F, Van Melderen L. 55.  2011. Toxins-antitoxins: diversity, evolution and function. Crit. Rev. Biochem. Mol. Biol. 46:386–408 [Google Scholar]
  56. He F, Chen L, Peng X. 56.  2014. First experimental evidence for the presence of a CRISPR toxin in Sulfolobus. J. Mol. Biol. 426:3683–88 [Google Scholar]
  57. He W, Huang T, Tang Y, Liu Y, Wu X. 57.  et al. 2015. Regulation of DNA phosphorothioate modification in Salmonella enterica by DndB. Sci. Rep. 5:12368 [Google Scholar]
  58. Hickman AB, Dyda F. 58.  2015. The casposon-encoded Cas1 protein from Aciduliprofundum boonei is a DNA integrase that generates target site duplications. Nucleic Acids Res 43:10576–87 [Google Scholar]
  59. Ho WS, Ou HY, Yeo CC, Thong KL. 59.  2015. The dnd operon for DNA phosphorothioation modification system in Escherichia coli is located in diverse genomic islands. BMC Genom 16:199 [Google Scholar]
  60. Hoskisson PA, Sumby P, Smith MC. 60.  2015. The phage growth limitation system in Streptomyces coelicolor A(3)2 is a toxin/antitoxin system, comprising enzymes with DNA methyltransferase, protein kinase and ATPase activity. Virology 477:100–9 [Google Scholar]
  61. Hu W, Wang C, Liang J, Zhang T, Hu Z. 61.  et al. 2012. Structural insights into DndE from Escherichia coli B7A involved in DNA phosphorothioation modification. Cell Res 22:1203–6 [Google Scholar]
  62. Hug LA, Baker BJ, Anantharaman K, Brown CT, Probst AJ. 62.  et al. 2016. A new view of the tree of life. Nat. Microbiol. 1:16048 [Google Scholar]
  63. Hur JK, Olovnikov I, Aravin AA. 63.  2014. Prokaryotic Argonautes defend genomes against invasive DNA. Trends Biochem. Sci. 39:257–59 [Google Scholar]
  64. Hutvagner G, Simard MJ. 64.  2008. Argonaute proteins: key players in RNA silencing. Nat. Rev. Mol. Cell Biol. 9:22–32 [Google Scholar]
  65. Hyman P, Abedon ST. 65.  2010. Bacteriophage host range and bacterial resistance. Adv. Appl. Microbiol. 70:217–48 [Google Scholar]
  66. Ichige A, Kobayashi I. 66.  2005. Stability of EcoRI restriction-modification enzymes in vivo differentiates the EcoRI restriction-modification system from other postsegregational cell killing systems. J. Bacteriol. 187:6612–21 [Google Scholar]
  67. Iranzo J, Lobkovsky AE, Wolf YI, Koonin EV. 67.  2013. Evolutionary dynamics of the prokaryotic adaptive immunity system CRISPR-Cas in an explicit ecological context. J. Bacteriol. 195:3834–44 [Google Scholar]
  68. Iranzo J, Puigbo P, Lobkovsky AE, Wolf YI, Koonin EV. 68.  2016. Inevitability of genetic parasites. Genome Biol. Evol. 8:2856–69 [Google Scholar]
  69. Jansen R, Embden JD, Gaastra W, Schouls LM. 69.  2002. Identification of genes that are associated with DNA repeats in prokaryotes. Mol. Microbiol. 43:1565–75 [Google Scholar]
  70. Ka D, Kim D, Baek G, Bae E. 70.  2014. Structural and functional characterization of Streptococcus pyogenes Cas2 protein under different pH conditions. Biochem. Biophys. Res. Commun. 451:152–7 [Google Scholar]
  71. Kapitonov VV, Makarova KS, Koonin EV. 71.  2015. ISC, a novel group of bacterial and archaeal DNA transposons that encode Cas9 homologs. J. Bacteriol. 198:797–807 [Google Scholar]
  72. Karginov FV, Hannon GJ. 72.  2010. The CRISPR system: small RNA-guided defense in bacteria and archaea. Mol. Cell 37:7–19 [Google Scholar]
  73. Kaufmann G. 73.  2000. Anticodon nucleases. Trends Biochem. Sci. 25:70–74 [Google Scholar]
  74. Kimelman A, Levy A, Sberro H, Kidron S, Leavitt A. 74.  et al. 2012. A vast collection of microbial genes that are toxic to bacteria. Genome Res 22:802–9 [Google Scholar]
  75. Klaiman D, Kaufmann G. 75.  2011. Phage T4-induced dTTP accretion bolsters a tRNase-based host defense. Virology 414:97–101 [Google Scholar]
  76. Klaiman D, Steinfels-Kohn E, Kaufmann G. 76.  2014. A DNA break inducer activates the anticodon nuclease RloC and the adaptive immunity in Acinetobacter baylyi ADP1. Nucleic Acids Res 42:328–39 [Google Scholar]
  77. Kobayashi I. 77.  2001. Behavior of restriction-modification systems as selfish mobile elements and their impact on genome evolution. Nucleic Acids Res 29:3742–56 [Google Scholar]
  78. Koonin EV. 78.  2016. Viruses and mobile elements as drivers of evolutionary transitions. Philos. Trans. R. Soc. Lond. B Biol. Sci. 371:20150442 [Google Scholar]
  79. Koonin EV. 79.  2017. Evolution of RNA- and DNA-guided antivirus defense systems in prokaryotes and eukaryotes: common ancestry vs convergence. Biol. Direct 12:5 [Google Scholar]
  80. Koonin EV, Dolja VV, Krupovic M. 80.  2015. Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479–480:2–25 [Google Scholar]
  81. Koonin EV, Krupovic M. 81.  2015. Evolution of adaptive immunity from transposable elements combined with innate immune systems. Nat. Rev. Genet. 16:184–92 [Google Scholar]
  82. Koonin EV, Krupovic M. 82.  2015. A movable defense. The Scientist, Jan. 1
  83. Koonin EV, Makarova KS. 83.  2009. CRISPR-Cas: an adaptive immunity system in prokaryotes. F1000 Biol. Rep. 1:95 [Google Scholar]
  84. Koonin EV, Wolf YI. 84.  2009. Is evolution Darwinian or/and Lamarckian?. Biol. Direct 4:42 [Google Scholar]
  85. Koonin EV, Wolf YI. 85.  2012. Evolution of microbes and viruses: a paradigm shift in evolutionary biology?. Front. Cell. Infect. Microbiol. 2:119 [Google Scholar]
  86. Koonin EV, Wolf YI. 86.  2015. Evolution of the CRISPR-Cas adaptive immunity systems in prokaryotes: models and observations on virus-host coevolution. Mol. Biosyst. 11:20–27 [Google Scholar]
  87. Koonin EV, Wolf YI. 87.  2016. Just how Lamarckian is CRISPR-Cas immunity: the continuum of evolvability mechanisms. Biol. Direct 11:9 [Google Scholar]
  88. Koonin EV, Zhang F. 88.  2017. Coupling immunity and programmed cell suicide in prokaryotes: life-or-death choices. BioEssays 39:1–9 [Google Scholar]
  89. Kovall RA, Matthews BW. 89.  1999. Type II restriction endonucleases: structural, functional and evolutionary relationships. Curr. Opin. Chem. Biol. 3:578–83 [Google Scholar]
  90. Krupovic M, Beguin P, Koonin EV. 90.  2017. Casposons: mobile genetic elements that gave rise to the CRISPR-Cas adaptation machinery. Curr. Opin. Microbiol. 38:36–43 [Google Scholar]
  91. Krupovic M, Koonin EV. 91.  2016. Self-synthesizing transposons: unexpected key players in the evolution of viruses and defense systems. Curr. Opin. Microbiol. 31:25–33 [Google Scholar]
  92. Krupovic M, Makarova KS, Forterre P, Prangishvili D, Koonin EV. 92.  2014. Casposons: a new superfamily of self-synthesizing DNA transposons at the origin of prokaryotic CRISPR-Cas immunity. BMC Biol 12:36 [Google Scholar]
  93. Krutkina E, Klaiman D, Margalit T, Jerabeck-Willemsen M, Kaufmann G. 93.  2016. Dual nucleotide specificity determinants of an infection aborting anticodon nuclease. Virology 487:260–72 [Google Scholar]
  94. Labrie SJ, Samson JE, Moineau S. 94.  2010. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8:317–27 [Google Scholar]
  95. Leplae R, Geeraerts D, Hallez R, Guglielmini J, Dreze P, Van Melderen L. 95.  2011. Diversity of bacterial type II toxin-antitoxin systems: a comprehensive search and functional analysis of novel families. Nucleic Acids Res 39:5513–25 [Google Scholar]
  96. Lingel A, Izaurralde E. 96.  2004. RNAi: finding the elusive endonuclease. RNA 10:1675–79 [Google Scholar]
  97. Liu J, Carmell MA, Rivas FV, Marsden CG, Thomson JM. 97.  et al. 2004. Argonaute2 is the catalytic engine of mammalian RNAi. Science 305:1437–41 [Google Scholar]
  98. Liu L, Li X, Wang J, Wang M, Chen P. 98.  et al. 2017. Two distant catalytic sites are responsible for C2c2 RNase activities. Cell 168:121–34 [Google Scholar]
  99. Loenen WA, Dryden DT, Raleigh EA, Wilson GG. 99.  2014. Type I restriction enzymes and their relatives. Nucleic Acids Res 42:20–44 [Google Scholar]
  100. Loenen WA, Raleigh EA. 100.  2014. The other face of restriction: modification-dependent enzymes. Nucleic Acids Res 42:56–69 [Google Scholar]
  101. Makarova KS, Anantharaman V, Aravind L, Koonin EV. 101.  2012. Live virus-free or die: Coupling of antivirus immunity and programmed suicide or dormancy in prokaryotes. Biol. Direct 7:40 [Google Scholar]
  102. Makarova KS, Anantharaman V, Grishin NV, Koonin EV, Aravind L. 102.  2014. CARF and WYL domains: ligand-binding regulators of prokaryotic defense systems. Front. Genet. 5:102 [Google Scholar]
  103. Makarova KS, Aravind L, Wolf YI, Koonin EV. 103.  2011. Unification of Cas protein families and a simple scenario for the origin and evolution of CRISPR-Cas systems. Biol. Direct 6:38 [Google Scholar]
  104. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV. 104.  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 [Google Scholar]
  105. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E. 105.  et al. 2011. Evolution and classification of the CRISPR-Cas systems. Nat. Rev. Microbiol. 9:467–77 [Google Scholar]
  106. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA. 106.  et al. 2015. An updated evolutionary classification of CRISPR-Cas systems. Nat. Rev. Microbiol. 13:722–36 [Google Scholar]
  107. Makarova KS, Wolf YI, Forterre P, Prangishvili D, Krupovic M, Koonin EV. 107.  2014. Dark matter in archaeal genomes: a rich source of novel mobile elements, defense systems and secretory complexes. Extremophiles 18:877–93 [Google Scholar]
  108. Makarova KS, Wolf YI, Koonin EV. 108.  2009. Comprehensive comparative-genomic analysis of type 2 toxin-antitoxin systems and related mobile stress response systems in prokaryotes. Biol. Direct 4:19 [Google Scholar]
  109. Makarova KS, Wolf YI, Koonin EV. 109.  2013. Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res 41:4360–77 [Google Scholar]
  110. Makarova KS, Wolf YI, Koonin EV. 110.  2013. The basic building blocks and evolution of CRISPR-Cas systems. Biochem. Soc. Trans. 41:1392–400 [Google Scholar]
  111. Makarova KS, Wolf YI, Snir S, Koonin EV. 111.  2011. Defense islands in bacterial and archaeal genomes and prediction of novel defense systems. J. Bacteriol. 193:6039–56 [Google Scholar]
  112. Makarova KS, Wolf YI, van der Oost J, Koonin EV. 112.  2009. Prokaryotic homologs of Argonaute proteins are predicted to function as key components of a novel system of defense against mobile genetic elements. Biol. Direct 4:29 [Google Scholar]
  113. Mohanraju P, Makarova KS, Zetsche B, Zhang F, Koonin EV, van der Oost J. 113.  2016. Diverse evolutionary roots and mechanistic variations of the CRISPR-Cas systems. Science 353:aad5147 [Google Scholar]
  114. Mojica FJ, Diez-Villasenor C, Garcia-Martinez J, Soria E. 114.  2005. Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J. Mol. Evol. 60:174–82 [Google Scholar]
  115. Mruk I, Kobayashi I. 115.  2014. To be or not to be: regulation of restriction-modification systems and other toxin-antitoxin systems. Nucleic Acids Res 42:70–86 [Google Scholar]
  116. Naito T, Kusano K, Kobayashi I. 116.  1995. Selfish behavior of restriction-modification systems. Science 267:897–99 [Google Scholar]
  117. Nakayama Y, Kobayashi I. 117.  1998. Restriction-modification gene complexes as selfish gene entities: Roles of a regulatory system in their establishment, maintenance, and apoptotic mutual exclusion. PNAS 95:6442–47 [Google Scholar]
  118. Nam KH, Ding F, Haitjema C, Huang Q, DeLisa MP, Ke A. 118.  2012. Double-stranded endonuclease activity in Bacillus halodurans clustered regularly interspaced short palindromic repeats (CRISPR)-associated Cas2 protein. J. Biol. Chem. 287:35943–52 [Google Scholar]
  119. Niewoehner O, Jinek M. 119.  2016. Structural basis for the endoribonuclease activity of the type III-A CRISPR-associated protein Csm6. RNA 22:318–29 [Google Scholar]
  120. Nunez JK, Kranzusch PJ, Noeske J, Wright AV, Davies CW, Doudna JA. 120.  2014. Cas1-Cas2 complex formation mediates spacer acquisition during CRISPR-Cas adaptive immunity. Nat. Struct. Mol. Biol. 21:528–34 [Google Scholar]
  121. Nunez JK, Lee AS, Engelman A, Doudna JA. 121.  2015. Integrase-mediated spacer acquisition during CRISPR-Cas adaptive immunity. Nature 519:193–98 [Google Scholar]
  122. Ohno S, Handa N, Watanabe-Matsui M, Takahashi N, Kobayashi I. 122.  2008. Maintenance forced by a restriction-modification system can be modulated by a region in its modification enzyme not essential for methyltransferase activity. J. Bacteriol. 190:2039–49 [Google Scholar]
  123. Oliveira PH, Touchon M, Rocha EP. 123.  2014. The interplay of restriction-modification systems with mobile genetic elements and their prokaryotic hosts. Nucleic Acids Res 42:10618–31 [Google Scholar]
  124. Oliveira PH, Touchon M, Rocha EP. 124.  2016. Regulation of genetic flux between bacteria by restriction-modification systems. PNAS 113:5658–63 [Google Scholar]
  125. Olovnikov I, Chan K, Sachidanandam R, Newman DK, Aravin AA. 125.  2013. Bacterial Argonaute samples the transcriptome to identify foreign DNA. Mol. Cell 51:594–605 [Google Scholar]
  126. Orlowski J, Bujnicki JM. 126.  2008. Structural and evolutionary classification of Type II restriction enzymes based on theoretical and experimental analyses. Nucleic Acids Res 36:3552–69 [Google Scholar]
  127. Otsuka Y. 127.  2016. Prokaryotic toxin-antitoxin systems: novel regulations of the toxins. Curr. Genet. 62:379–82 [Google Scholar]
  128. Page R, Peti W. 128.  2016. Toxin-antitoxin systems in bacterial growth arrest and persistence. Nat. Chem. Biol. 12:208–14 [Google Scholar]
  129. Parker JS, Barford D. 129.  2006. Argonaute: a scaffold for the function of short regulatory RNAs. Trends Biochem. Sci. 31:622–30 [Google Scholar]
  130. Parker JS, Roe SM, Barford D. 130.  2005. Structural insights into mRNA recognition from a PIWI domain-siRNA guide complex. Nature 434:663–66 [Google Scholar]
  131. Pasternak C, Dulermo R, Ton-Hoang B, Debuchy R, Siguier P. 131.  et al. 2013. ISDra2 transposition in Deinococcus radiodurans is downregulated by TnpB. Mol. Microbiol. 88:443–55 [Google Scholar]
  132. Pingoud A, Wilson GG, Wende W. 132.  2014. Type II restriction endonucleases—a historical perspective and more. Nucleic Acids Res 42:7489–527 Erratum 2016. Nucleic Acids Res 44:8011 [Google Scholar]
  133. Puigbò P, Lobkovsky AE, Kristensen DM, Wolf YI, Koonin EV. 133.  2014. Genomes in turmoil: quantification of genome dynamics in prokaryote supergenomes. BMC Biol 12:66 [Google Scholar]
  134. Puigbò P, Makarova KS, Kristensen DM, Wolf YI, Koonin EV. 134.  2017. Reconstruction of the evolution of microbial defense systems. BMC Evol. Biol. 17:94 [Google Scholar]
  135. Qi L, Haurwitz RE, Shao W, Doudna JA, Arkin AP. 135.  2012. RNA processing enables predictable programming of gene expression. Nat. Biotechnol. 30:1002–6 [Google Scholar]
  136. Rao DN, Dryden DT, Bheemanaik S. 136.  2014. Type III restriction-modification enzymes: a historical perspective. Nucleic Acids Res 42:45–55 [Google Scholar]
  137. Rimer J, Cohen IR, Friedman N. 137.  2014. Do all creatures possess an acquired immune system of some sort?. BioEssays 36:273–81 [Google Scholar]
  138. Roberts RJ, Belfort M, Bestor T, Bhagwat AS, Bickle TA. 138.  et al. 2003. A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res 31:1805–12 [Google Scholar]
  139. Roberts RJ, Vincze T, Posfai J, Macelis D. 139.  2007. REBASE–enzymes and genes for DNA restriction and modification. Nucleic Acids Res 35:D269–70 [Google Scholar]
  140. Rohwer F, Thurber RV. 140.  2009. Viruses manipulate the marine environment. Nature 459:207–12 [Google Scholar]
  141. Rusinov I, Ershova A, Karyagina A, Spirin S, Alexeevski A. 141.  2015. Lifespan of restriction-modification systems critically affects avoidance of their recognition sites in host genomes. BMC Genom 16:1084 [Google Scholar]
  142. Sberro H, Leavitt A, Kiro R, Koh E, Peleg Y. 142.  et al. 2013. Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning. Mol. Cell 50:136–48 [Google Scholar]
  143. Seed KD, Lazinski DW, Calderwood SB, Camilli A. 143.  2013. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494:489–91 [Google Scholar]
  144. Sheng G, Zhao H, Wang J, Rao Y, Tian W. 144.  et al. 2014. Structure-based cleavage mechanism of Thermus thermophilus Argonaute DNA guide strand-mediated DNA target cleavage. PNAS 111:652–57 [Google Scholar]
  145. Sheppard NF, Glover CV 3rd, Terns RM, Terns MP. 145.  2016. The CRISPR-associated Csx1 protein of Pyrococcus furiosus is an adenosine-specific endoribonuclease. RNA 22:216–24 [Google Scholar]
  146. Shmakov S, Abudayyeh OO, Makarova KS, Wolf YI, Gootenberg JS. 146.  et al. 2015. Discovery and functional characterization of diverse class 2 CRISPR-Cas systems. Mol. Cell 60:385–97 [Google Scholar]
  147. Shmakov S, Smargon A, Scott D, Cox D, Pyzocha N. 147.  et al. 2017. Diversity and evolution of class 2 CRISPR-Cas systems. Nat. Rev. Microbiol. 15:169–82 [Google Scholar]
  148. Silas S, Mohr G, Sidote DJ, Markham LM, Sanchez-Amat A. 148.  et al. 2016. Direct CRISPR spacer acquisition from RNA by a natural reverse transcriptase-Cas1 fusion protein. Science 351:aad4234 [Google Scholar]
  149. Smargon AA, Cox DB, Pyzocha NK, Zheng K, Slaymaker IM. 149.  et al. 2017. Cas13b is a type VI-B CRISPR-associated RNA-guided RNase differentially regulated by accessory proteins Csx27 and Csx28. Mol. Cell 65:618–30.e7 [Google Scholar]
  150. Song JJ, Smith SK, Hannon GJ, Joshua-Tor L. 150.  2004. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305:1434–37 [Google Scholar]
  151. Stern A, Sorek R. 151.  2011. The phage-host arms race: shaping the evolution of microbes. BioEssays 33:43–51 [Google Scholar]
  152. Sternberg SH, Richter H, Charpentier E, Qimron U. 152.  2016. Adaptation in CRISPR-Cas systems. Mol. Cell 61:797–808 [Google Scholar]
  153. Sumby P, Smith MC. 153.  2002. Genetics of the phage growth limitation (Pgl) system of Streptomyces coelicolor A3(2). Mol. Microbiol. 44:489–500 [Google Scholar]
  154. Suttle CA. 154.  2005. Viruses in the sea. Nature 437:356–61 [Google Scholar]
  155. Suttle CA. 155.  2007. Marine viruses—major players in the global ecosystem. Nat. Rev. Microbiol. 5:801–12 [Google Scholar]
  156. Swarts DC, Hegge JW, Hinojo I, Shiimori M, Ellis MA. 156.  et al. 2015. Argonaute of the archaeon Pyrococcus furiosus is a DNA-guided nuclease that targets cognate DNA. Nucleic Acids Res 43:5120–29 [Google Scholar]
  157. Swarts DC, Jore MM, Westra ER, Zhu Y, Janssen JH. 157.  et al. 2014. DNA-guided DNA interference by a prokaryotic Argonaute. Nature 507:258–61 [Google Scholar]
  158. Swarts DC, Makarova K, Wang Y, Nakanishi K, Ketting RF. 158.  et al. 2014. The evolutionary journey of Argonaute proteins. Nat. Struct. Mol. Biol. 21:743–53 [Google Scholar]
  159. Syed MA, Levesque CM. 159.  2012. Chromosomal bacterial type II toxin-antitoxin systems. Can. J. Microbiol. 58:553–62 [Google Scholar]
  160. Szathmary E, Maynard Smith J. 160.  1997. From replicators to reproducers: the first major transitions leading to life. J. Theor. Biol. 187:555–71 [Google Scholar]
  161. Tabara H, Sarkissian M, Kelly WG, Fleenor J, Grishok A. 161.  et al. 1999. The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99:123–32 [Google Scholar]
  162. Tan Q, Awano N, Inouye M. 162.  2011. YeeV is an Escherichia coli toxin that inhibits cell division by targeting the cytoskeleton proteins, FtsZ and MreB. Mol. Microbiol. 79:109–18 [Google Scholar]
  163. Tock MR, Dryden DT. 163.  2005. The biology of restriction and anti-restriction. Curr. Opin. Microbiol. 8:466–72 [Google Scholar]
  164. Toussaint A, Chandler M. 164.  2012. Prokaryote genome fluidity: toward a system approach of the mobilome. Methods Mol. Biol. 804:57–80 [Google Scholar]
  165. Uzan M. 165.  2009. RNA processing and decay in bacteriophage T4. Prog. Mol. Biol. Transl. Sci. 85:43–89 [Google Scholar]
  166. van der Oost J, Jore MM, Westra ER, Lundgren M, Brouns SJ. 166.  2009. CRISPR-based adaptive and heritable immunity in prokaryotes. Trends Biochem. Sci. 34:401–7 [Google Scholar]
  167. Van Melderen L. 167.  2010. Toxin-antitoxin systems: why so many, what for?. Curr. Opin. Microbiol. 13:781–85 [Google Scholar]
  168. Van Melderen L, Saavedra De Bast M. 168.  2009. Bacterial toxin-antitoxin systems: more than selfish entities?. PLOS Genet 5:e1000437 [Google Scholar]
  169. Wang C, Villion M, Semper C, Coros C, Moineau S, Zimmerly S. 169.  2011. A reverse transcriptase-related protein mediates phage resistance and polymerizes untemplated DNA in vitro. Nucleic Acids Res 39:7620–29 [Google Scholar]
  170. Wang Y, Juranek S, Li H, Sheng G, Tuschl T, Patel DJ. 170.  2008. Structure of an Argonaute silencing complex with a seed-containing guide DNA and target RNA duplex. Nature 456:921–26 [Google Scholar]
  171. Weinberger AD, Wolf YI, Lobkovsky AE, Gilmore MS, Koonin EV. 171.  2012. Viral diversity threshold for adaptive immunity in prokaryotes. mBio 3:e00456–12 [Google Scholar]
  172. Westra ER, Buckling A, Fineran PC. 172.  2014. CRISPR-Cas systems: beyond adaptive immunity. Nat. Rev. Microbiol. 12:317–26 [Google Scholar]
  173. Westra ER, Swarts DC, Staals RH, Jore MM, Brouns SJ, van der Oost J. 173.  2012. The CRISPRs, they are a-changin’: how prokaryotes generate adaptive immunity. Annu. Rev. Genet. 46:311–39 [Google Scholar]
  174. Wiedenheft B, Sternberg SH, Doudna JA. 174.  2012. RNA-guided genetic silencing systems in bacteria and archaea. Nature 482:331–38 [Google Scholar]
  175. Williams RJ. 175.  2003. Restriction endonucleases: classification, properties, and applications. Mol. Biotechnol. 23:225–43 [Google Scholar]
  176. Willkomm S, Zander A, Grohmann D, Restle T. 176.  2016. Mechanistic insights into archaeal and human Argonaute substrate binding and cleavage properties. PLOS ONE 11:e0164695 [Google Scholar]
  177. Xiong W, Zhao G, Yu H, He X. 177.  2015. Interactions of Dnd proteins involved in bacterial DNA phosphorothioate modification. Front. Microbiol. 6:1139 [Google Scholar]
  178. Xu T, Liang J, Chen S, Wang L, He X. 178.  et al. 2009. DNA phosphorothioation in Streptomyces lividans: mutational analysis of the dnd locus. BMC Microbiol 9:41 [Google Scholar]
  179. Yamaguchi Y, Inouye M. 179.  2009. mRNA interferases, sequence-specific endoribonucleases from the toxin-antitoxin systems. Prog. Mol. Biol. Transl. Sci. 85:467–500 [Google Scholar]
  180. Yamaguchi Y, Park JH, Inouye M. 180.  2011. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45:61–79 [Google Scholar]
  181. Yamano T, Nishimasu H, Zetsche B, Hirano H, Slaymaker IM. 181.  et al. 2016. Crystal structure of Cpf1 in complex with guide RNA and target DNA. Cell 165:949–62 [Google Scholar]
  182. Yang H, Gao P, Rajashankar KR, Patel DJ. 182.  2016. PAM-dependent target DNA recognition and cleavage by C2c1 CRISPR-Cas endonuclease. Cell 167:1814–28.e12 [Google Scholar]
  183. Yao J, Guo Y, Zeng Z, Liu X, Shi F, Wang X. 183.  2015. Identification and characterization of a HEPN-MNT family type II toxin-antitoxin in Shewanella oneidensis. Microb. Biotechnol. 8:961–73 [Google Scholar]
  184. You D, Wang L, Yao F, Zhou X, Deng Z. 184.  2007. A novel DNA modification by sulfur: DndA is a NifS-like cysteine desulfurase capable of assembling DndC as an iron-sulfur cluster protein in Streptomyces lividans. Biochemistry 46:6126–33 [Google Scholar]
  185. Yuan YR, Pei Y, Ma JB, Kuryavyi V, Zhadina M. 185.  et al. 2005. Crystal structure of A. aeolicus Argonaute, a site-specific DNA-guided endoribonuclease, provides insights into RISC-mediated mRNA cleavage. Mol. Cell 19:405–19 [Google Scholar]
  186. Zalatan JG, Fenn TD, Herschlag D. 186.  2008. Comparative enzymology in the alkaline phosphatase superfamily to determine the catalytic role of an active-site metal ion. J. Mol. Biol. 384:1174–89 [Google Scholar]
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Evolutionary Genomics of Defense Systems in Archaea and Bacteria*
Annual Review of Microbiology 71, 233 (2017); https://doi.org/10.1146/annurev-micro-090816-093830
/content/journals/10.1146/annurev-micro-090816-093830
/content/journals/10.1146/annurev-micro-090816-093830
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