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Marine Microbe Stress Responses to Bacteriophage Infection

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Abstract

Bacteriophages are bacteria-specific viral predators and exist wherever bacteria thrive. In order to evade phage infection and killing, bacteria have evolved diverse defense strategies. Phages rapidly coevolve with their hosts to overcome the obstacles of host defense systems, resulting in a constant molecular arms race. The extensive coevolution of both phage and host has led to considerable diversity of both bacterial and phage defensive and offensive strategies. This predator-prey dynamic equilibrium has several profound impacts, ranging from global nutrient cycling, to human health and disease, and to food and biotechnology industries. In this chapter, we highlight the antiviral mechanisms of bacteria that act at every stage of phage life cycle, including phage adsorption and DNA injection interference, phage assembly interference, restriction-modification systems, abortive infection systems, and CRISPR systems.

Keywords

Bacteriophage Antiviral strategy Stress response 

References

  1. Allers T, Mevarech M (2005) Archaeal genetics – the third way. Nat Rev Genet 6:58–73PubMedCrossRefGoogle Scholar
  2. Allison GE, Klaenhammer TR (1998) Phage resistance mechanisms in lactic acid bacteria. Int Dairy J 8:207–226CrossRefGoogle Scholar
  3. Altemeier WA, Lewis SA, Schlievert PM, Bergdoll MS, Bjornson HS, Staneck JL, Crass BA (1982) Staphylococcus aureus associated with toxic shock syndrome: phage typing and toxin capability testing. Ann Intern Med 96(6_Part_2):978–982PubMedCrossRefGoogle Scholar
  4. Amitai G, Sorek R (2016) CRISPR-Cas adaptation: insights into the mechanism of action. Nat Rev Microbiol 14:67–76PubMedCrossRefGoogle Scholar
  5. Antunes LCM, Ferreira RB, Buckner MM, Finlay BB (2010) Quorum sensing in bacterial virulence. Microbiology 156:2271–2282PubMedCrossRefGoogle Scholar
  6. Atanasiu C, Su TJ, Sturrock S, Dryden D (2002) Interaction of the ocr gene 0.3 protein of bacteriophage T7 with Eco KI restriction/modification enzyme. Nucleic Acids Res 30:3936–3944PubMedPubMedCentralCrossRefGoogle Scholar
  7. Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D (2011) Genomic island variability facilitates Prochlorococcus–virus coexistence. Nature 474:604CrossRefGoogle Scholar
  8. Bair CL, Black LW (2007) A type IV modification dependent restriction nuclease that targets glucosylated hydroxymethyl cytosine modified DNAs. J Mol Biol 366:768–778PubMedCrossRefGoogle Scholar
  9. Bair CL, Rifat D, Black LW (2007) Exclusion of glucosyl-hydroxymethylcytosine DNA containing bacteriophages is overcome by the injected protein inhibitor IPI. J Mol Biol 366:779–789PubMedCrossRefGoogle Scholar
  10. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero D, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709PubMedCrossRefGoogle Scholar
  11. Bebeacua C, Lorenzo Fajardo JC, Blangy S, Spinelli S, Bollmann S, Neve H, Cambillau C, Heller KJ (2013) X-ray structure of a superinfection exclusion lipoprotein from phage TP-J 34 and identification of the tape measure protein as its target. Mol Microbiol 89:152–165PubMedCrossRefGoogle Scholar
  12. Bento JC, Lane KD, Read EK, Cerca N, Christie GE (2014) Sequence determinants for DNA packaging specificity in the Staphylococcus aureus pathogenicity island SaPI1. Plasmid 71:8–15PubMedCrossRefGoogle Scholar
  13. Bergdoll M, Reiser R, Crass B, Robbins R, Davis J (1981) A new staphylococcal enterotoxin, enterotoxin F, associated with toxic-shock-syndrome Staphylococcus aureus isolates. Lancet 317(8228):1017–1021CrossRefGoogle Scholar
  14. Bertani G, Weigle J (1953) Host controlled variation in bacterial viruses. J Bacteriol 65:113PubMedPubMedCentralGoogle Scholar
  15. Bickle TA (2004) Restricting restriction. Mol Microbiol 51:3–5PubMedCrossRefGoogle Scholar
  16. Bidnenko E, Ehrlich D, Chopin M (1995) Phage operon involved in sensitivity to the Lactococcus lactis abortive infection mechanism AbiD1. J Bacteriol 177:3824–3829PubMedPubMedCentralCrossRefGoogle Scholar
  17. Bidnenko E, Ehrlich S, Chopin M (1998) Lactococcus lactis phage operon coding for an endonuclease homologous to RuvC. Mol Microbiol 28:823–834PubMedCrossRefGoogle Scholar
  18. Bidnenko E, Chopin M, Ehrlich S, Anba J (2002) Lactococcus lactis AbiD1 abortive infection efficiency is drastically increased by a phage protein. FEMS Microbiol Lett 214:283–287PubMedCrossRefGoogle Scholar
  19. Bidnenko E, Chopin A, Ehrlich S, Chopin M (2009) Activation of mRNA translation by phage protein and low temperature: the case of Lactococcus lactis abortive infection system AbiD1. BMC Mol Biol 10:4PubMedPubMedCentralCrossRefGoogle Scholar
  20. Bikard D, Marraffini LA (2012) Innate and adaptive immunity in bacteria: mechanisms of programmed genetic variation to fight bacteriophages. Curr Opin Immunol 24:15–20PubMedCrossRefGoogle Scholar
  21. Blaseio U, Pfeifer F (1990) Transformation of Halobacterium halobium: development of vectors and investigation of gas vesicle synthesis. Proc Natl Acad Sci U S A 87:6772–6776PubMedPubMedCentralCrossRefGoogle Scholar
  22. Blosser TR, Loeff L, Westra ER, Vlot M, Kunne T, Sobota M, Dekker C, Brouns SJJ, Joo C (2015) Two distinct DNA binding modes guide dual roles of a CRISPR-Cas protein complex. Mol Cell 58:60–70PubMedPubMedCentralCrossRefGoogle Scholar
  23. Blower TR, Chai R, Przybilski R, Chindhy S, Fang X, Kidman SE, Tan H, Luisi BF, Fineran PC, Salmond GP (2017) Evolution of Pectobacterium bacteriophage PhiM1 to escape two bifunctional type III toxin-antitoxin and abortive infection systems through mutations in a single viral gene. Appl Environ Microbiol 83:e03229PubMedPubMedCentralCrossRefGoogle Scholar
  24. Bolotin A, Quinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:2551–2561PubMedCrossRefGoogle Scholar
  25. Botelho A, Canto A, Leao C, Cunha MV (2015) Clustered regularly interspaced short palindromic repeats (CRISPRs) analysis of members of the Mycobacterium tuberculosis complex. Methods Mol Biol 1247:373–389PubMedCrossRefGoogle Scholar
  26. Bouchard JD, Moineau S (2004) Lactococcal phage genes involved in sensitivity to AbiK and their relation to single-strand annealing proteins. J Bacteriol 186:3649–3652PubMedPubMedCentralCrossRefGoogle Scholar
  27. Bouchard JD, Dion E, Bissonnette F, Moineau S (2002) Characterization of the two-component abortive phage infection mechanism AbiT from Lactococcus lactis. J Bacteriol 184:6325–6332PubMedPubMedCentralCrossRefGoogle Scholar
  28. Boulnois G, Roberts I (1990) Genetics of capsular polysaccharide production in bacteria. In: Bacterial capsules. Springer, LondonGoogle Scholar
  29. Breitbart M (2012) Marine viruses: truth or dare. Annu Rev Mar Sci 4:425–448CrossRefGoogle Scholar
  30. Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ, Snijders AP, Dickman MJ, Makarova KS, Koonin EV, van der Oost J (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960–964PubMedPubMedCentralCrossRefGoogle Scholar
  31. Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG, Alberti A, Chaffron S, Cruaud C, de Vargas C, Gasol JM, Gorsky G, Gregory AC, Guidi L, Hingamp P, Iudicone D, Not F, Ogata H, Pesant S, Poulos BT, Schwenck SM, Speich S, Dimier C, Kandels-Lewis S, Picheral M, Searson S, Tara Oceans C, Bork P, Bowler C, Sunagawa S, Wincker P, Karsenti E, Sullivan MB (2015) Ocean plankton. Patterns and ecological drivers of ocean viral communities. Science 348:1261498CrossRefGoogle Scholar
  32. Carte J, Wang R, Li H, Terns RM, Terns MP (2008) Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev 22:3489–3496PubMedPubMedCentralCrossRefGoogle Scholar
  33. Castillo FJ, Bartell PF (1974) Studies on the bacteriophage 2 receptors of Pseudomonas aeruginosa. J Virol 14:904–909PubMedPubMedCentralGoogle Scholar
  34. Chen Y, Wei D, Wang Y, Zhang X (2013) The role of interactions between bacterial chaperone, aspartate aminotransferase, and viral protein during virus infection in high temperature environment: the interactions between bacterium and virus proteins. BMC Microbiol 13:48PubMedPubMedCentralCrossRefGoogle Scholar
  35. Chinen A, Uchiyama I, Kobayashi I (2000) Comparison between Pyrococcus horikoshii and Pyrococcus abyssi genome sequences reveals linkage of restriction–modification genes with large genome polymorphisms. Gene 259:109–121PubMedCrossRefGoogle Scholar
  36. Chopin M-C, Chopin A, Bidnenko E (2005) Phage abortive infection in lactococci: variations on a theme. Curr Opin Microbiol 8:473–479PubMedCrossRefGoogle Scholar
  37. Christie GE, Dokland T (2012) Pirates of the Caudovirales. Virology 434:210–221PubMedPubMedCentralCrossRefGoogle Scholar
  38. Chu MC, Kreiswirth BN, Pattee PA, Novick RP, Melish ME, James JF (1988) Association of toxic shock toxin-1 determinant with a heterologous insertion at multiple loci in the Staphylococcus aureus chromosome. Infect Immun 56(10):2702–2708PubMedPubMedCentralGoogle Scholar
  39. 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 339:819–823PubMedPubMedCentralCrossRefGoogle Scholar
  40. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penades JR (2001) Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J Bacteriol 183:2888–2896PubMedPubMedCentralCrossRefGoogle Scholar
  41. Dai G, Su P, Allison GE, Geller BL, Zhu P, Kim WS, Dunn NW (2001) Molecular characterization of a new abortive infection system (AbiU) from Lactococcus lactis LL51-1. Appl Environ Microbiol 67:5225–5232PubMedPubMedCentralCrossRefGoogle Scholar
  42. Damle PK, Wall EA, Spilman MS, Dearborn AD, Ram G, Novick RP, Dokland T, Christie GE (2012) The roles of SaPI1 proteins gp7 (CpmA) and gp6 (CpmB) in capsid size determination and helper phage interference. Virology 432:277–282PubMedPubMedCentralCrossRefGoogle Scholar
  43. Dearborn AD, Spilman MS, Damle PK, Chang JR, Monroe EB, Saad JS, Christie GE, Dokland T (2011) The Staphylococcus aureus pathogenicity island 1 protein gp6 functions as an internal scaffold during capsid size determination. J Mol Biol 412:710–722PubMedPubMedCentralCrossRefGoogle Scholar
  44. Deltcheva E, Chylinski K, Sharma CM, Gonzales K, Chao Y, Pirzada ZA, Eckert MR, Vogel J, Charpentier E (2011) CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III. Nature 471:602–607PubMedPubMedCentralCrossRefGoogle Scholar
  45. Destoumieux-Garzón D, Peduzzi J, Rebuffat S (2002) Focus on modified microcins: structural features and mechanisms of action. Biochimie 84:511–519PubMedCrossRefGoogle Scholar
  46. Destoumieux-Garzón D, Duquesne S, Peduzzi J, Goulard C, Desmadril M, Letellier L, Rebuffat S, Boulanger P (2005) The iron–siderophore transporter FhuA is the receptor for the antimicrobial peptide microcin J25: role of the microcin Val11–Pro16 β-hairpin region in the recognition mechanism. Biochem J 389:869–876PubMedPubMedCentralCrossRefGoogle Scholar
  47. Deveau H, Barrangou R, Garneau JE, Labonte J, Fremaux C, Boyaval P, Romero DA, Horvath P, Moineau S (2008) Phage response to CRISPR-encoded resistance in Streptococcus thermophilus. J Bacteriol 190:1390–1400PubMedCrossRefGoogle Scholar
  48. Domingues S, McGovern S, Plochocka D, Santos M, Ehrlich S, Polard P, Chopin M (2008) The lactococcal abortive infection protein AbiP is membrane-anchored and binds nucleic acids. Virology 373:14–24PubMedCrossRefGoogle Scholar
  49. Dong Y, Kumar CG, Chia N, Kim PJ, Miller PA, Price ND, Cann IK, Flynn TM, Sanford RA, Krapac IG, Locke RA 2nd, Hong PY, Tamaki H, Liu WT, Mackie RI, Hernandez AG, Wright CL, Mikel MA, Walker JL, Sivaguru M, Fried G, Yannarell AC, Fouke BW (2014) Halomonas sulfidaeris-dominated microbial community inhabits a 1.8 km-deep subsurface Cambrian Sandstone reservoir. Environ Microbiol 16:1695–1708PubMedCrossRefGoogle Scholar
  50. Dryden D, Murray NE, Rao D (2001) Nucleoside triphosphate-dependent restriction enzymes. Nucleic Acids Res 29:3728–3741PubMedPubMedCentralCrossRefGoogle Scholar
  51. Durmaz E, Klaenhammer T (2007) Abortive phage resistance mechanism AbiZ speeds the lysis clock to cause premature lysis of phage-infected Lactococcus lactis. J Bacteriol 189:1417–1425PubMedCrossRefGoogle Scholar
  52. Dy R, Przybilski R, Semeijn K, Salmond G, Fineran P (2014a) A widespread bacteriophage abortive infection system functions through a Type IV toxin-antitoxin mechanism. Nucleic Acids Res 42:4590–4605PubMedPubMedCentralCrossRefGoogle Scholar
  53. Dy RL, Richter C, Salmond GPC, Fineran PC (2014b) Remarkable mechanisms in microbes to resist phage infections. Annu Rev Virol 1(1):307–331PubMedCrossRefGoogle Scholar
  54. Emond E, Holler BJ, Boucher I, Vandenbergh PA, Vedamuthu ER, Kondo JK, Moineau S (1997) Phenotypic and genetic characterization of the bacteriophage abortive infection mechanism AbiK from Lactococcus lactis. Appl Environ Microbiol 63:1274–1283PubMedPubMedCentralGoogle Scholar
  55. Emond E, Dion E, Walker SA, Vedamuthu ER, Kondo JK, Moineau S (1998) AbiQ, an abortive infection mechanism from Lactococcus lactis. Appl Environ Microbiol 64:4748–4756PubMedPubMedCentralGoogle Scholar
  56. Feiss M, Rao VB (2012) The bacteriophage DNA packaging machine. Adv Exp Med Biol 726:489–509PubMedCrossRefGoogle Scholar
  57. Ferrer MD, Quiles-Puchalt N, Harwich MD, Tormo-Mas MA, Campoy S, Barbe J, Lasa I, Novick RP, Christie GE, Penades JR (2011) RinA controls phage-mediated packaging and transfer of virulence genes in Gram-positive bacteria. Nucleic Acids Res 39:5866–5878PubMedPubMedCentralCrossRefGoogle Scholar
  58. Fillol-Salom A, Martínez-Rubio R, Abdulrahman RF, Chen J, Davies R, Penadés JR (2018) Phage-inducible chromosomal islands are ubiquitous within the bacterial universe. ISME J 12:2114PubMedPubMedCentralCrossRefGoogle Scholar
  59. Fineran P, Blower T, Foulds I, Humphreys D, Lilley K, Salmond G (2009) The phage abortive infection system, ToxIN, functions as a protein-RNA toxin-antitoxin pair. Proc Natl Acad Sci U S A 106:894–899PubMedPubMedCentralCrossRefGoogle Scholar
  60. Fitzgerald JR, Monday SR, Foster TJ, Bohach GA, Hartigan PJ, Meaney WJ, Smyth CJ (2001) Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J Bacteriol 183:63–70PubMedPubMedCentralCrossRefGoogle Scholar
  61. Forde A, Fitzgerald GF (1999) Bacteriophage defence systems in lactic acid bacteria. Lactic acid bacteria: genetics. Metabolism and applications. Springer, DordrechtGoogle Scholar
  62. Fortier LC, Bouchard JD, Moineau S (2005) Expression and site-directed mutagenesis of the lactococcal abortive phage infection protein AbiK. J Bacteriol 187:3721–3730PubMedPubMedCentralCrossRefGoogle Scholar
  63. Galperin MY, Koonin EV (2000) Who’s your neighbor? New computational approaches for functional genomics. Nat Biotechnol 18:609PubMedCrossRefGoogle Scholar
  64. Gasiunas G, Barrangou R, Horvath P, Siksnys V (2012) Cas9-crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria. Proc Natl Acad Sci 109:E2579–E2586PubMedCrossRefGoogle Scholar
  65. Godde JS, Bickerton A (2006) The repetitive DNA elements called CRISPRs and their associated genes: evidence of horizontal transfer among prokaryotes. J Mol Evol 62:718–729PubMedCrossRefGoogle Scholar
  66. Goldberg GW, Jiang W, Bikard D, Marraffini LA (2014) Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting. Nature 514:633–637PubMedPubMedCentralCrossRefGoogle Scholar
  67. Grissa I, Vergnaud G, Pourcel C (2007) The CRISPRdb database and tools to display CRISPRs and to generate dictionaries of spacers and repeats. BMC Bioinf 8:172CrossRefGoogle Scholar
  68. Grogan DW (2003) Cytosine methylation by the SuaI restriction-modification system: implications for genetic fidelity in a hyperthermophilic archaeon. J Bacteriol 185:4657–4661PubMedPubMedCentralCrossRefGoogle Scholar
  69. Guerrero-Ferreira RC, Viollier PH, Ely B, Poindexter JS, Georgieva M, Jensen GJ, Wright ER (2011) Alternative mechanism for bacteriophage adsorption to the motile bacterium Caulobacter crescentus. Proc Natl Acad Sci 108:9963–9968PubMedCrossRefGoogle Scholar
  70. Hale CR, Zhao P, Olson S, Duff MO, Graveley BR, Wells L, Terns RM, Terns MP (2009) RNA-guided RNA cleavage by a CRISPR RNA-Cas protein complex. Cell 139:945–956PubMedPubMedCentralCrossRefGoogle Scholar
  71. Hanlon GW, Denyer SP, Olliff CJ, Ibrahim LJ (2001) Reduction in exopolysaccharide viscosity as an aid to bacteriophage penetration through Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 67:2746–2753PubMedPubMedCentralCrossRefGoogle Scholar
  72. Haurwitz RE, Jinek M, Wiedenheft B, Zhou K, Doudna JA (2010) Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329:1355–1358PubMedPubMedCentralCrossRefGoogle Scholar
  73. He T, Li H, Zhang X (2017) Deep-sea hydrothermal vent viruses compensate for microbial metabolism in virus-host interactions. MBio 8:e00893PubMedPubMedCentralCrossRefGoogle Scholar
  74. Hermans PW, van Soolingen D, Bik EM, de Haas PE, Dale JW, van Embden JD (1991) Insertion element IS987 from Mycobacterium bovis BCG is located in a hot-spot integration region for insertion elements in Mycobacterium tuberculosis complex strains. Infect Immun 59:2695–2705PubMedPubMedCentralGoogle Scholar
  75. Hershey AD (1971) The bacteriophage lambda. Cold Spring Harbor Laboratory, Cold Spring HarborGoogle Scholar
  76. Hill C (1993) Bacteriophage and bacteriophage resistance in lactic acid bacteria. FEMS Microbiol Rev 12:87–108CrossRefGoogle Scholar
  77. Hill C, Miller L, Klaenhammer T (1990) Nucleotide sequence and distribution of the pTR2030 resistance determinant (hsp) which aborts bacteriophage infection in lactococci. Appl Environ Microbiol 56:2255–2258PubMedPubMedCentralGoogle Scholar
  78. Horvath P (2008) Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 190:1401PubMedCrossRefGoogle Scholar
  79. Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167–170PubMedPubMedCentralCrossRefGoogle Scholar
  80. Høyland-Kroghsbo NM, Mærkedahl RB, Svenningsen SL (2013) A quorum-sensing-induced bacteriophage defense mechanism. MBio 4:e00362–e00312PubMedPubMedCentralCrossRefGoogle Scholar
  81. Huang CX, Zhang YY, Jiao NZ (2010) Phage resistance of a marine bacterium, Roseobacter denitrificans OCh114, as revealed by comparative proteomics. Curr Microbiol 61:141–147PubMedCrossRefGoogle Scholar
  82. Hur JK, Olovnikov I, Aravin AA (2014) Prokaryotic argonautes defend genomes against invasive DNA. Trends Biochem Sci 39:257–259PubMedPubMedCentralCrossRefGoogle Scholar
  83. Hynes WL, Hancock L, Ferretti JJ (1995) Analysis of a second bacteriophage hyaluronidase gene from Streptococcus pyogenes: evidence for a third hyaluronidase involved in extracellular enzymatic activity. Infect Immun 63:3015–3020PubMedPubMedCentralGoogle Scholar
  84. 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 Bacteriol 169:5429–5433PubMedPubMedCentralCrossRefGoogle Scholar
  85. Jansen R, Embden JDV, Gaastra W, Schouls LM (2002a) Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43:1565–1575PubMedCrossRefGoogle Scholar
  86. Jansen R, van Embden JD, Gaastra W, Schouls LM (2002b) Identification of a novel family of sequence repeats among prokaryotes. OMICS 6:23PubMedCrossRefGoogle Scholar
  87. Jeffreys AJ, MacLeod A, Tamaki K, Neil DL, Monckton DG (1991) Minisatellite repeat coding as a digital approach to DNA typing. Nature 354:204–209PubMedCrossRefGoogle Scholar
  88. Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31:233–239PubMedPubMedCentralCrossRefGoogle Scholar
  89. Jin M, Chen Y, Xu C, Zhang X (2014) The effect of inhibition of host MreB on the infection of thermophilic phage GVE2 in high temperature environment. Sci Rep 4:4823PubMedPubMedCentralCrossRefGoogle Scholar
  90. Jin M, Xu C, Zhang X (2015) The effect of tryptophol on the bacteriophage infection in high-temperature environment. Appl Microbiol Biotechnol 99:8101–8111PubMedCrossRefGoogle Scholar
  91. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337:816–821PubMedPubMedCentralCrossRefGoogle Scholar
  92. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J (2013) RNA-programmed genome editing in human cells. elife 2:e00471PubMedPubMedCentralCrossRefGoogle Scholar
  93. Jore MM, Lundgren M, van Duijn E, Bultema JB, Westra ER, Waghmare SP, Wiedenheft B, Pul U, Wurm R, Wagner R, Beijer MR, Barendregt A, Zhou K, Snijders AP, Dickman MJ, Doudna JA, Boekema EJ, Heck AJ, van der Oost J, Brouns SJ (2011) Structural basis for CRISPR RNA-guided DNA recognition by Cascade. Nat Struct Mol Biol 18:529–536PubMedCrossRefGoogle Scholar
  94. Joung JK, Voytas DF, Kamens J (2015) Accelerating research through reagent repositories: the genome editing example. Genome Biol 16:255PubMedPubMedCentralCrossRefGoogle Scholar
  95. Kao C, Snyder L (1988) The lit gene product which blocks bacteriophage T4 late gene expression is a membrane protein encoded by a cryptic DNA element, e14. J Bacteriol 170:2056–2062PubMedPubMedCentralCrossRefGoogle Scholar
  96. Kaufmann G, David M, Borasio GD, Teichmann A, Paz A, Amitsur M, Green R, Snyder L (1986) Phage and host genetic determinants of the specific anticodon loop cleavages in bacteriophage T4-infected Escherichia coli CTr5X. J Mol Biol 188:15–22PubMedCrossRefGoogle Scholar
  97. Kliem M, Dreiseikelmann B (1989) The superimmunity gene sim of bacteriophage P1 causes superinfection exclusion. Virology 171:350–355PubMedCrossRefGoogle Scholar
  98. Koonin EV, Makarova KS, Wolf YI (2017) Evolutionary genomics of defense systems in archaea and bacteria. Annu Rev Microbiol 71:233–261PubMedPubMedCentralCrossRefGoogle Scholar
  99. Kreiswirth BN, Projan SJ, Schlievert PM, Novick RP (1989) Toxic shock syndrome toxin 1 is encoded by a variable genetic element. Rev Infect Dis 11(Suppl. 1):S83–S88PubMedCrossRefGoogle Scholar
  100. Krüger D, Bickle TA (1983) Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic acid restriction systems of their hosts. Microbiol Rev 47:345PubMedPubMedCentralGoogle Scholar
  101. Krüger D, Barcak G, Smith H (1988) Abolition of DNA recognition site resistance to the restriction endonuclease EcoRII. Biomed Biochim Acta 47:K1–K5PubMedGoogle Scholar
  102. Kunin V, Sorek R, Hugenholtz P (2007) Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol 8:R61PubMedPubMedCentralCrossRefGoogle Scholar
  103. Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327CrossRefGoogle Scholar
  104. Levitz R, Chapman D, Amitsur M, Green R, Snyder L, Kaufmann G (1990) The optional E. coli prr locus encodes a latent form of phage T4-induced anticodon nuclease. EMBO J 9:1383–1389PubMedPubMedCentralCrossRefGoogle Scholar
  105. Lin LF, Posfai J, Roberts RJ, Kong H (2001) Comparative genomics of the restriction-modification systems in Helicobacter pylori. Proc Natl Acad Sci 98:2740–2745PubMedCrossRefGoogle Scholar
  106. Lindqvist BH, Deho G, Calendar R (1993) Mechanisms of genome propagation and helper exploitation by satellite phage P4. Microbiol Rev 57:683–702PubMedPubMedCentralGoogle Scholar
  107. Lindsay JA, Ruzin A, Ross HF, Kurepina N, Novick RP (1998) The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol 29:527–543PubMedCrossRefGoogle Scholar
  108. Liu B, Wu S, Song Q, Xie L, Zhang X (2006) Two novel bacteriophages of thermophilic bacteria isolated from deep-sea hydrothermal fields. Curr Microbiol 53:163–166CrossRefGoogle Scholar
  109. Loenen WA (2003) Tracking EcoKI and DNA fifty years on: a golden story full of surprises. Nucleic Acids Res 31:7059–7069PubMedPubMedCentralCrossRefGoogle Scholar
  110. Lu MJ, Henning U (1994) Superinfection exclusion by T-even-type coliphages. Trends Microbiol 2:137–139PubMedCrossRefGoogle Scholar
  111. Lu M, Stierhof Y, Henning U (1993) Location and unusual membrane topology of the immunity protein of the Escherichia coli phage T4. J Virol 67:4905–4913PubMedPubMedCentralGoogle Scholar
  112. Magnuson R (2007) Hypothetical functions of toxin-antitoxin systems. J Bacteriol 189:6089–6092PubMedPubMedCentralCrossRefGoogle Scholar
  113. Mahony J, McGrath S, Fitzgerald GF, van Sinderen D (2008) Identification and characterization of lactococcal-prophage-carried superinfection exclusion genes. Appl Environ Microbiol 74:6206–6215PubMedPubMedCentralCrossRefGoogle Scholar
  114. Maillou J, Dreiseikelmann B (1990) The sim gene of Escherichia coli phage P1: nucleotide sequence and purification of the processed protein. Virology 175:500–507PubMedCrossRefGoogle Scholar
  115. Maiques E, Ubeda C, Tormo MA, Ferrer MD, Lasa I, Novick RP, Penades JR (2007) Role of staphylococcal phage and SaPI integrase in intra- and interspecies SaPI transfer. J Bacteriol 189:5608–5616PubMedPubMedCentralCrossRefGoogle Scholar
  116. Makarova KS, Aravind L, Grishin NV, Rogozin IB, Koonin EV (2002) A DNA repair system specific for thermophilic Archaea and bacteria predicted by genomic context analysis. Nucleic Acids Res 30:482–496PubMedPubMedCentralCrossRefGoogle Scholar
  117. Makarova KS, Wolf YI, Koonin EV (2013) Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res 41:4360–4377PubMedPubMedCentralCrossRefGoogle Scholar
  118. Makarova KS, Haft DH, Barrangou R, Brouns SJ, Charpentier E, Horvath P, Moineau S, Mojica FJ, Wolf YI, Yakunin AF (2011) Evolution and classification of the CRISPR–Cas systems. Nat Rev Microbiol 9:467CrossRefGoogle Scholar
  119. Makarova KS, Wolf YI, Alkhnbashi OS, Costa F, Shah SA, Saunders SJ, Barrangou R, Brouns SJ, Charpentier E, Haft DH, Horvath P, Moineau S, Mojica FJ, Terns RM, Terns MP, White MF, Yakunin AF, Garrett RA, van der Oost J, Backofen R, Koonin EV (2015) An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol 13:722–736PubMedPubMedCentralCrossRefGoogle Scholar
  120. 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 339:823–826PubMedPubMedCentralCrossRefGoogle Scholar
  121. Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–1845PubMedPubMedCentralCrossRefGoogle Scholar
  122. Martinez-Rubio R, Quiles-Puchalt N, Marti M, Humphrey S, Ram G, Smyth D, Chen J, Novick RP, Penades JR (2017) Phage-inducible islands in the Gram-positive cocci. ISME J 11:1029–1042PubMedCrossRefGoogle Scholar
  123. Mathavan I, Beis K (2012) The role of bacterial membrane proteins in the internalization of microcin MccJ25 and MccB17. Portland Press LimitedGoogle Scholar
  124. Merino S, Camprubi S, Tomás JM (1990) Isolation and characterization of bacteriophage PM3 from Aeromonas hydrophila the bacterial receptor for which is the monopolar flagellum. FEMS Microbiol Lett 69:277–282CrossRefGoogle Scholar
  125. Meyer JL, Huber JA (2014) Strain-level genomic variation in natural populations of Lebetimonas from an erupting deep-sea volcano. ISME J 8:867–880PubMedCrossRefGoogle Scholar
  126. Moak M, Molineux IJ (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51:1169–1183PubMedCrossRefGoogle Scholar
  127. Mojica FJ, Juez G, Rodriguez-Valera F (1993) Transcription at different salinities of Haloferax mediterranei sequences adjacent to partially modified PstI sites. Mol Microbiol 9:613–621PubMedCrossRefGoogle Scholar
  128. Mojica FJ, Ferrer C, Juez G, Rodriguez-Valera F (1995) Long stretches of short tandem repeats are present in the largest replicons of the Archaea Haloferax mediterranei and Haloferax volcanii and could be involved in replicon partitioning. Mol Microbiol 17:85–93PubMedCrossRefGoogle Scholar
  129. Mojica FJ, Diez-Villasenor C, Soria E, Juez G (2000) Biological significance of a family of regularly spaced repeats in the genomes of Archaea, Bacteria and mitochondria. Mol Microbiol 36:244–246PubMedCrossRefGoogle Scholar
  130. 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 60:174–182PubMedCrossRefGoogle Scholar
  131. Morgan R, Xiao J, Xu S (1998) Characterization of an extremely thermostable restriction enzyme, PspGI, from a Pyrococcus strain and cloning of the PspGI restriction-modification system in Escherichia coli. Appl Environ Microbiol 64:3669–3673PubMedPubMedCentralGoogle Scholar
  132. Moses AE, Wessels MR, Zalcman K, Albertí S, Natanson-Yaron S, Menes T, Hanski E (1997) Relative contributions of hyaluronic acid capsule and M protein to virulence in a mucoid strain of the group A Streptococcus. Infect Immun 65:64–71PubMedPubMedCentralGoogle Scholar
  133. Mosig G, Lin G, Franklin J, Fan W (1989) Functional relationships and structural determinants of two bacteriophage T4 lysozymes: a soluble (gene e) and a baseplate-associated (gene 5) protein. New Biol 1:171–179PubMedGoogle Scholar
  134. Murray NE (2000) Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol Mol Biol Rev 64:412–434PubMedPubMedCentralCrossRefGoogle Scholar
  135. Nakata A, Amemura M, Makino K (1989) Unusual nucleotide arrangement with repeated sequences in the Escherichia coli K-12 chromosome. J Bacteriol 171:3553–3556PubMedPubMedCentralCrossRefGoogle Scholar
  136. Nolling J, de Vos WM (1992) Characterization of the archaeal, plasmid-encoded type II restriction-modification system MthTI from Methanobacterium thermoformicicum THF: homology to the bacterial NgoPII system from Neisseria gonorrhoeae. J Bacteriol 174:5719–5726PubMedPubMedCentralCrossRefGoogle Scholar
  137. Nölling J, de Vos WM (1992) Identification of the CTAG-recognizing restriction-modification systems MthZI and MthFI from Methanobacterium thermoformicicum and characterization of the plasmid-encoded mthZIM gene. Nucleic Acids Res 20:5047–5052PubMedPubMedCentralCrossRefGoogle Scholar
  138. Novick RP, Christie GE, Penades JR (2010) The phage-inducible chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8:541–551PubMedPubMedCentralCrossRefGoogle Scholar
  139. O’Connor L, Tangney M, Fitzgerald GF (1999) Expression, regulation, and mode of action of the AbiG abortive infection system of lactococcus lactis subsp. cremoris UC653. Appl Environ Microbiol 65:330–335PubMedPubMedCentralGoogle Scholar
  140. O’sullivan D, Twomey DP, Coffey A, Hill C, Fitzgerald GF, Ross RP (2000) Novel type I restriction specificities through domain shuffling of HsdS subunits in Lactococcus lactis. Mol Microbiol 36:866–875PubMedCrossRefGoogle Scholar
  141. Parma DH, Snyder M, Sobolevski S, Nawroz M, Brody E, Gold L (1992) The Rex system of bacteriophage lambda: tolerance and altruistic cell death. Genes Dev 6:497–510PubMedCrossRefGoogle Scholar
  142. Penadés JR, Christie GE (2015) The phage-inducible chromosomal islands: a family of highly evolved molecular parasites. Annu Rev Virol 2:181–201PubMedCrossRefGoogle Scholar
  143. Penadés JR, Chen J, Quiles-Puchalt N, Carpena N, Novick RP (2015) Bacteriophage-mediated spread of bacterial virulence genes. Curr Opin Microbiol 23:171–178CrossRefGoogle Scholar
  144. Pingoud A (2012) Restriction endonucleases. Springer, BerlinGoogle Scholar
  145. Pingoud A, Fuxreiter M, Pingoud V, Wende W (2005) Type II restriction endonucleases: structure and mechanism. Cell Mol Life Sci 62:685PubMedCrossRefGoogle Scholar
  146. Poliakov A, Chang JR, Spilman MS, Damle PK, Christie GE, Mobley JA, Dokland T (2008) Capsid size determination by Staphylococcus aureus pathogenicity island SaPI1 involves specific incorporation of SaPI1 proteins into procapsids. J Mol Biol 380:465–475PubMedPubMedCentralCrossRefGoogle Scholar
  147. Qin QL, Li Y, Zhang YJ, Zhou ZM, Zhang WX, Chen XL, Zhang XY, Zhou BC, Wang L, Zhang YZ (2011) Comparative genomics reveals a deep-sea sediment-adapted life style of Pseudoalteromonas sp. SM9913. ISME J 5:274–284PubMedCrossRefGoogle Scholar
  148. Quiles PN, Mart´ ınez-Rubio R, Ram G, Lasa I, Penades JR (2014) Unravelling bacteriophage ϕ11 requirements for packaging and transfer of mobile genetic elements in Staphylococcus aureus. Mol Microbiol 91:423–437CrossRefGoogle Scholar
  149. Quiles-Puchalt N, Tormo-Mas MA, Campoy S, Toledo-Arana A, Monedero V, Lasa I, Novick RP, Christie GE, Penades JR (2013) A super-family of transcriptional activators regulates bacteriophage packaging and lysis in Gram-positive bacteria. Nucleic Acids Res 41:7260–7275PubMedPubMedCentralCrossRefGoogle Scholar
  150. Raleigh EA, Wilson G (1986) Escherichia coli K-12 restricts DNA containing 5-methylcytosine. Proc Natl Acad Sci 83:9070–9074PubMedCrossRefGoogle Scholar
  151. Ram G, Chen J, Kumar K, Ross HF, Ubeda C, Damle PK, Lane KD, Penades JR, Christie GE, Novick RP (2012) Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism. Proc Natl Acad Sci U S A 109:16300–16305PubMedPubMedCentralCrossRefGoogle Scholar
  152. Ram G, Chen J, Ross HF, Novick RP (2014) Precisely modulated pathogenicity island interference with late phage gene transcription. Proc Natl Acad Sci U S A 111:14536–14541PubMedPubMedCentralCrossRefGoogle Scholar
  153. Rifat D, Wright NT, Varney KM, Weber DJ, Black LW (2008) Restriction endonuclease inhibitor IPI* of bacteriophage T4: a novel structure for a dedicated target. J Mol Biol 375:720–734PubMedCrossRefGoogle Scholar
  154. Ripp S, Miller RV (1998) Dynamics of the pseudolysogenic response in slowly growing cells of Pseudomonas aeruginosa. Microbiology 144:2225–2232PubMedCrossRefPubMedCentralGoogle Scholar
  155. Roberts RJ, Belfort M, Bestor T, Bhagwat AS, Bickle TA, Bitinaite J, Blumenthal RM, Degtyarev SK, Dryden DT, Dybvig K (2003) A nomenclature for restriction enzymes, DNA methyltransferases, homing endonucleases and their genes. Nucleic Acids Res 31:1805–1812PubMedPubMedCentralCrossRefGoogle Scholar
  156. Roberts RJ, Vincze T, Posfai J, Macelis D (2014) REBASE—a database for DNA restriction and modification: enzymes, genes and genomes. Nucleic Acids Res 43:D298–DD99PubMedPubMedCentralCrossRefGoogle Scholar
  157. Rodriguez-Brito B, Li L, Wegley L, Furlan M, Angly F, Breitbart M, Buchanan J, Desnues C, Dinsdale E, Edwards R (2010) Viral and microbial community dynamics in four aquatic environments. ISME J 4:739PubMedPubMedCentralCrossRefGoogle Scholar
  158. Roux S, Brum JR, Dutilh BE, Sunagawa S, Duhaime MB, Loy A, Poulos BT, Solonenko N, Lara E, Poulain J, Pesant S, Kandels-Lewis S, Dimier C, Picheral M, Searson S, Cruaud C, Alberti A, Duarte CM, Gasol JM, Vaque D, Tara Oceans C, Bork P, Acinas SG, Wincker P, Sullivan MB (2016) Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537:689–693PubMedCrossRefGoogle Scholar
  159. Ruzin A, Lindsay J, Novick RP (2001) Molecular genetics of SaPI1-a mobile pathogenicity island in Staphylococcus aureus. Mol Microbiol 41:365–377PubMedCrossRefPubMedCentralGoogle Scholar
  160. Samson JE, Magadán AH, Sabri M, Moineau S (2013) Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 11:675CrossRefGoogle Scholar
  161. Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32:347–355PubMedPubMedCentralCrossRefGoogle Scholar
  162. Sapranauskas R, Gasiunas G, Fremaux C, Barrangou R, Horvath P, Siksnys V (2011) The Streptococcus thermophilus CRISPR/Cas system provides immunity in Escherichia coli. Nucleic Acids Res 39:9275–9282PubMedPubMedCentralCrossRefGoogle Scholar
  163. Sashital DG, Wiedenheft B, Doudna JA (2012) Mechanism of foreign DNA selection in a bacterial adaptive immune system. Mol Cell 46:606–615PubMedPubMedCentralCrossRefGoogle Scholar
  164. Schlievert PM, Shands KN, Dan BB, Schmid GP, Nishimura RD (1981) Identification and characterization of an exotoxin from Staphylococcus aureus associated with toxic-shock syndrome. J Infect Dis 143:509–516PubMedCrossRefPubMedCentralGoogle Scholar
  165. Schnabel H, Zillig W, Pfaffle M, Schnabel R, Michel H, Delius H (1982) Halobacterium halobium phage oH. EMBO J 1:87–92PubMedPubMedCentralCrossRefGoogle Scholar
  166. Seed KD (2015) Battling phages: how bacteria defend against viral attack. PLoS Pathog 11:e1004847PubMedPubMedCentralCrossRefGoogle Scholar
  167. 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 108:10098–10103PubMedPubMedCentralCrossRefGoogle Scholar
  168. Shen B, Zhang J, Wu H, Wang J, Ma K, Li Z, Zhang X, Zhang P, Huang X (2013) Generation of gene-modified mice via Cas9/RNA-mediated gene targeting. Cell Res 23:720–723PubMedPubMedCentralCrossRefGoogle Scholar
  169. Sinkunas T, Gasiunas G, Waghmare SP, Dickman MJ, Barrangou R, Horvath P, Siksnys V (2013) In vitro reconstitution of Cascade-mediated CRISPR immunity in Streptococcus thermophilus. EMBO J 32:385–394PubMedPubMedCentralCrossRefGoogle Scholar
  170. Snyder L (1995) Phage-exclusion enzymes: a bonanza of biochemical and cell biology reagents? Mol Microbiol 15:415–420PubMedCrossRefGoogle Scholar
  171. Snyder L, McWilliams K (1989) The rex genes of bacteriophage lambda can inhibit cell function without phage superinfection. Gene 81:17–24PubMedCrossRefGoogle Scholar
  172. Sokolowski RD, Graham S, White MF (2014) Cas6 specificity and CRISPR RNA loading in a complex CRISPR-Cas system. Nucleic Acids Res 42:6532–6541PubMedPubMedCentralCrossRefGoogle Scholar
  173. Sorek R, Kunin V, Hugenholtz P (2008) CRISPR – a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6:181PubMedCrossRefGoogle Scholar
  174. Spilman MS, Dearborn AD, Chang JR, Damle PK, Christie GE, Dokland T (2011) A conformational switch involved in maturation of Staphylococcus aureus bacteriophage 80α capsids. J Mol Biol 405:863–876PubMedCrossRefGoogle Scholar
  175. Staals RH, Zhu Y, Taylor DW, Kornfeld JE, Sharma K, Barendregt A, Koehorst JJ, Vlot M, Neupane N, Varossieau K, Sakamoto K, Suzuki T, Dohmae N, Yokoyama S, Schaap PJ, Urlaub H, Heck AJ, Nogales E, Doudna JA, Shinkai A, van der Oost J (2014) RNA targeting by the type III-A CRISPR-Cas Csm complex of Thermus thermophilus. Mol Cell 56:518–530PubMedPubMedCentralCrossRefGoogle Scholar
  176. Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA (2014) DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507:62–67PubMedPubMedCentralCrossRefGoogle Scholar
  177. Stewart FJ, Panne D, Bickle TA, Raleigh EA (2000) Methyl-specific DNA binding by McrBC, a modification-dependent restriction enzyme 1. J Mol Biol 298:611–622PubMedCrossRefGoogle Scholar
  178. Stirm S (1968) Escherichia coli K bacteriophages I. isolation and introductory characterization of five Escherichia coli K bacteriophages. J Virol 2:1107–1114PubMedPubMedCentralGoogle Scholar
  179. Stoddard LI, Martiny JB, Marston MF (2007) Selection and characterization of cyanophage resistance in marine Synechococcus strains. Appl Environ Microbiol 73:5516–5522PubMedPubMedCentralCrossRefGoogle Scholar
  180. Sun X, Göhler A, Heller KJ, Neve H (2006) The ltp gene of temperate Streptococcus thermophilus phage TP-J34 confers superinfection exclusion to Streptococcus thermophilus and Lactococcus lactis. Virology 350:146–157PubMedCrossRefGoogle Scholar
  181. Sutherland IW (1995) Polysaccharide lyases. FEMS Microbiol Rev 16:323–347PubMedCrossRefGoogle Scholar
  182. Suttle CA (2007) Marine viruses--major players in the global ecosystem. Nat Rev Microbiol 5:801–812PubMedPubMedCentralCrossRefGoogle Scholar
  183. Tallent SM, Christie GE (2007) Transducing particles of Staphylococcus aureus pathogenicity island SaPI1are comprised of helper phage-encoded proteins. J Bacteriol 189:7520–7524PubMedPubMedCentralCrossRefGoogle Scholar
  184. Tamulaitis G, Kazlauskiene M, Manakova E, Venclovas C, Nwokeoji AO, Dickman MJ, Horvath P, Siksnys V (2014) Programmable RNA shredding by the type III-A CRISPR-Cas system of Streptococcus thermophilus. Mol Cell 56:506–517PubMedCrossRefGoogle Scholar
  185. Temple G, Ayling P, Wilkinson S (1986) Isolation and characterization of a lipopolysaccharide-specific bacteriophage of Pseudomonas aeruginosa. Microbios 45:81–91PubMedGoogle Scholar
  186. Tock MR, Dryden DT (2005) The biology of restriction and anti-restriction. Curr Opin Microbiol 8:466–472PubMedCrossRefGoogle Scholar
  187. Tormo MA, Ferrer MD, Maiques E, Ubeda C, Selva L, Lasa I, Calvete JJ, Novick RP, Penades JR (2008) Staphylococcus aureus pathogenicity island DNA is packaged in particles composed of phage proteins. J Bacteriol 190:2434–2440PubMedPubMedCentralCrossRefGoogle Scholar
  188. Ubeda C, Tormo MA, Cucarella C, Trotonda P, Foster TJ, Lasa I, Penades JR (2003) Sip, an integrase protein with excision, circularization and integration activities, defines a new family of mobile Staphylococcus aureus pathogenicity islands. Mol Microbiol 49:193–210PubMedCrossRefGoogle Scholar
  189. Ubeda C, Maiques E, Knecht E, Lasa I, Novick RP, Penades JR (2005) Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol Microbiol 56:836–844CrossRefGoogle Scholar
  190. Ubeda C, Maiques E, Tormo MA, Campoy S, Lasa I, Barbe J, Novick RP, Penades JR (2007) SaPI operon I is required for SaPI packaging and is controlled by LexA. Mol Microbiol 65:41–50PubMedCrossRefGoogle Scholar
  191. Ubeda C, Olivarez NP, Barry P, Wang H, Kong XP, Matthews A, Tallent SM, Christie GE, Novick RP (2009) Specificity of staphylococcal phage and SaPI DNA packaging as revealed by integrase and terminase mutations. Mol Microbiol 72:98–108PubMedPubMedCentralCrossRefGoogle Scholar
  192. Vasu K, Nagaraja V (2013) Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol Mol Biol Rev 77:53–72PubMedPubMedCentralCrossRefGoogle Scholar
  193. Vovis GF, Lacks S (1977) Complementary action of restriction enzymes endo R· DpnI and endo R· DpnII on bacteriophage f1 DNA. J Mol Biol 115:525–538PubMedCrossRefGoogle Scholar
  194. Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914PubMedCrossRefGoogle Scholar
  195. Walkinshaw M, Taylor P, Sturrock S, Atanasiu C, Berge T, Henderson R, Edwardson J, Dryden D (2002) Structure of Ocr from bacteriophage T7, a protein that mimics B-form DNA. Mol Cell 9:187–194PubMedCrossRefGoogle Scholar
  196. Wang Y, Zhang X (2010) Genome analysis of deep-sea thermophilic phage D6E. Appl Environ Microbiol 76:7861–7866PubMedPubMedCentralCrossRefGoogle Scholar
  197. Wang H, Yang H, Shivalila CS, Dawlaty MM, Cheng AW, Zhang F, Jaenisch R (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–918PubMedPubMedCentralCrossRefGoogle Scholar
  198. Wei D, Zhang X (2010) Proteomic analysis of interactions between a deep-sea thermophilic bacteriophage and its host at high temperature. J Virol 84:2365–2373CrossRefGoogle Scholar
  199. Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181PubMedPubMedCentralCrossRefGoogle Scholar
  200. Wiedenheft B, van Duijn E, Bultema JB, Waghmare SP, Zhou K, Barendregt A, Westphal W, Heck AJ, Boekema EJ, Dickman MJ, Doudna JA (2011) RNA-guided complex from a bacterial immune system enhances target recognition through seed sequence interactions. Proc Natl Acad Sci U S A 108:10092–10097PubMedPubMedCentralCrossRefGoogle Scholar
  201. Williams P, Cámara M (2009) Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules. Curr Opin Microbiol 12:182–191PubMedCrossRefGoogle Scholar
  202. Winter C, Bouvier T, Weinbauer MG, Thingstad TF (2010) Trade-offs between competition and defense specialists among unicellular planktonic organisms: the “killing the winner” hypothesis revisited. Microbiol Mol Biol Rev 74:42–57PubMedPubMedCentralCrossRefGoogle Scholar
  203. Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114PubMedPubMedCentralCrossRefGoogle Scholar
  204. Wyszomirski KH, Curth U, Alves J, Mackeldanz P, Möncke-Buchner E, Schutkowski M, Krüger DH, Reuter M (2011) Type III restriction endonuclease EcoP15I is a heterotrimeric complex containing one Res subunit with several DNA-binding regions and ATPase activity. Nucleic Acids Res 40:3610–3622PubMedPubMedCentralCrossRefGoogle Scholar
  205. Yamaguchi Y, Park JH, Inouye M (2011) Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 45:61–79PubMedCrossRefGoogle Scholar
  206. Yang H, Wang H, Shivalila CS, Cheng AW, Shi L, Jaenisch R (2013) One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154:1370–1379PubMedPubMedCentralCrossRefGoogle Scholar
  207. Yokota S, Hayashi T, Matsumoto H (1994) Identification of the lipopolysaccharide core region as the receptor site for a cytotoxin-converting phage, phi CTX, of Pseudomonas aeruginosa. J Bacteriol 176:5262–5269PubMedPubMedCentralCrossRefGoogle Scholar
  208. Yu Y, Snyder L (1994) Translation elongation factor Tu cleaved by a phage-exclusion system. Proc Natl Acad Sci 91:802–806PubMedCrossRefGoogle Scholar
  209. Zebec Z, Manica A, Zhang J, White MF, Schleper C (2014) CRISPR-mediated targeted mRNA degradation in the archaeon Sulfolobus solfataricus. Nucleic Acids Res 42:5280–5288PubMedPubMedCentralCrossRefGoogle Scholar
  210. Zegans ME, Wagner JC, Cady KC, Murphy DM, Hammond JH, O’Toole GA (2009) Interaction between bacteriophage DMS3 and host CRISPR region inhibits group behaviors of Pseudomonas aeruginosa. J Bacteriol 191:210–219PubMedCrossRefGoogle Scholar
  211. Zhang Y, Jiao N (2009) Roseophage RDJLΦ1, infecting the aerobic anoxygenic phototrophic bacterium Roseobacter denitrificans OCh114. Appl Environ Microbiol 75:1745–1749PubMedPubMedCentralCrossRefGoogle Scholar
  212. Zhang J, Li W, Zhang Q, Wang H, Xu X, Diao B, Zhang L, Kan B (2009) The core oligosaccharide and thioredoxin of Vibrio cholerae are necessary for binding and propagation of its typing phage VP3. J Bacteriol 191:2622–2629PubMedPubMedCentralCrossRefGoogle Scholar
  213. Zhang Y, Huang C, Yang J, Jiao N (2011) Interactions between marine microorganisms and their phages. Chin Sci Bull 56:1770CrossRefGoogle Scholar
  214. Makarova K S, Haft D H, Barrangou R, Brouns S J, Charpentier E, Horvath P, Moineau S, Mojica F J, Wolf Y I, and Yakunin A F (2011) Evolution and classification of the CRISPR–Cas systems, Nature Reviews Microbiology, 9: 467PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  1. 1.Key Laboratory of Marine Genetic Resource, Third Institute of OceanographyMinistry of Natural ResourcesXiamenChina
  2. 2.Institute of Oceanology and College of Animal SciencesFujian Agriculture and Forestry UniversityFuzhouChina
  3. 3.College of Life SciencesZhejiang UniversityHangzhouChina

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