Skip to main content

Marine Microbe Stress Responses to Bacteriophage Infection

  • Chapter
  • First Online:
Book cover Virus Infection and Tumorigenesis

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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Allers T, Mevarech M (2005) Archaeal genetics – the third way. Nat Rev Genet 6:58–73

    Article  CAS  PubMed  Google Scholar 

  • Allison GE, Klaenhammer TR (1998) Phage resistance mechanisms in lactic acid bacteria. Int Dairy J 8:207–226

    Article  Google Scholar 

  • 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):978–982

    Article  CAS  PubMed  Google Scholar 

  • Amitai G, Sorek R (2016) CRISPR-Cas adaptation: insights into the mechanism of action. Nat Rev Microbiol 14:67–76

    Article  CAS  PubMed  Google Scholar 

  • Antunes LCM, Ferreira RB, Buckner MM, Finlay BB (2010) Quorum sensing in bacterial virulence. Microbiology 156:2271–2282

    Article  CAS  PubMed  Google Scholar 

  • 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 30:3936–3944

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Avrani S, Wurtzel O, Sharon I, Sorek R, Lindell D (2011) Genomic island variability facilitates Prochlorococcus–virus coexistence. Nature 474:604

    Article  CAS  PubMed  Google Scholar 

  • Bair CL, Black LW (2007) A type IV modification dependent restriction nuclease that targets glucosylated hydroxymethyl cytosine modified DNAs. J Mol Biol 366:768–778

    Article  CAS  PubMed  Google Scholar 

  • 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 366:779–789

    Article  CAS  PubMed  Google Scholar 

  • 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 315:1709

    Article  CAS  PubMed  Google Scholar 

  • 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 89:152–165

    Article  CAS  PubMed  Google Scholar 

  • 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 71:8–15

    Article  CAS  PubMed  Google Scholar 

  • 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):1017–1021

    Article  Google Scholar 

  • Bertani G, Weigle J (1953) Host controlled variation in bacterial viruses. J Bacteriol 65:113

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bickle TA (2004) Restricting restriction. Mol Microbiol 51:3–5

    Article  CAS  PubMed  Google Scholar 

  • Bidnenko E, Ehrlich D, Chopin M (1995) Phage operon involved in sensitivity to the Lactococcus lactis abortive infection mechanism AbiD1. J Bacteriol 177:3824–3829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bidnenko E, Ehrlich S, Chopin M (1998) Lactococcus lactis phage operon coding for an endonuclease homologous to RuvC. Mol Microbiol 28:823–834

    Article  CAS  PubMed  Google Scholar 

  • 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 214:283–287

    Article  CAS  PubMed  Google Scholar 

  • 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 10:4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bikard D, Marraffini LA (2012) Innate and adaptive immunity in bacteria: mechanisms of programmed genetic variation to fight bacteriophages. Curr Opin Immunol 24:15–20

    Article  CAS  PubMed  Google Scholar 

  • 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 87:6772–6776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 58:60–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e03229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolotin A, Quinquis B, Sorokin A, Ehrlich SD (2005) Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 151:2551–2561

    Article  CAS  PubMed  Google Scholar 

  • 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 1247:373–389

    Article  PubMed  Google Scholar 

  • Bouchard JD, Moineau S (2004) Lactococcal phage genes involved in sensitivity to AbiK and their relation to single-strand annealing proteins. J Bacteriol 186:3649–3652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouchard JD, Dion E, Bissonnette F, Moineau S (2002) Characterization of the two-component abortive phage infection mechanism AbiT from Lactococcus lactis. J Bacteriol 184:6325–6332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boulnois G, Roberts I (1990) Genetics of capsular polysaccharide production in bacteria. In: Bacterial capsules. Springer, London

    Google Scholar 

  • Breitbart M (2012) Marine viruses: truth or dare. Annu Rev Mar Sci 4:425–448

    Article  Google Scholar 

  • 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 321:960–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 348:1261498

    Article  CAS  PubMed  Google Scholar 

  • 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 22:3489–3496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castillo FJ, Bartell PF (1974) Studies on the bacteriophage 2 receptors of Pseudomonas aeruginosa. J Virol 14:904–909

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 13:48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 259:109–121

    Article  CAS  PubMed  Google Scholar 

  • Chopin M-C, Chopin A, Bidnenko E (2005) Phage abortive infection in lactococci: variations on a theme. Curr Opin Microbiol 8:473–479

    Article  CAS  PubMed  Google Scholar 

  • Christie GE, Dokland T (2012) Pirates of the Caudovirales. Virology 434:210–221

    Article  CAS  PubMed  Google Scholar 

  • 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):2702–2708

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 183:2888–2896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 67:5225–5232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 432:277–282

    Article  CAS  PubMed  Google Scholar 

  • 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 412:710–722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 471:602–607

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Destoumieux-Garzón D, Peduzzi J, Rebuffat S (2002) Focus on modified microcins: structural features and mechanisms of action. Biochimie 84:511–519

    Article  PubMed  Google Scholar 

  • 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 389:869–876

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 190:1390–1400

    Article  CAS  PubMed  Google Scholar 

  • 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 373:14–24

    Article  CAS  PubMed  Google Scholar 

  • 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 16:1695–1708

    Article  CAS  PubMed  Google Scholar 

  • Dryden D, Murray NE, Rao D (2001) Nucleoside triphosphate-dependent restriction enzymes. Nucleic Acids Res 29:3728–3741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 189:1417–1425

    Article  CAS  PubMed  Google Scholar 

  • 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 42:4590–4605

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dy RL, Richter C, Salmond GPC, Fineran PC (2014b) Remarkable mechanisms in microbes to resist phage infections. Annu Rev Virol 1(1):307–331

    Article  PubMed  CAS  Google Scholar 

  • 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 63:1274–1283

    CAS  PubMed  PubMed Central  Google Scholar 

  • Emond E, Dion E, Walker SA, Vedamuthu ER, Kondo JK, Moineau S (1998) AbiQ, an abortive infection mechanism from Lactococcus lactis. Appl Environ Microbiol 64:4748–4756

    CAS  PubMed  PubMed Central  Google Scholar 

  • Feiss M, Rao VB (2012) The bacteriophage DNA packaging machine. Adv Exp Med Biol 726:489–509

    Article  CAS  PubMed  Google Scholar 

  • 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 39:5866–5878

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 12:2114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 106:894–899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 183:63–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forde A, Fitzgerald GF (1999) Bacteriophage defence systems in lactic acid bacteria. Lactic acid bacteria: genetics. Metabolism and applications. Springer, Dordrecht

    Google Scholar 

  • Fortier LC, Bouchard JD, Moineau S (2005) Expression and site-directed mutagenesis of the lactococcal abortive phage infection protein AbiK. J Bacteriol 187:3721–3730

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galperin MY, Koonin EV (2000) Who’s your neighbor? New computational approaches for functional genomics. Nat Biotechnol 18:609

    Article  CAS  PubMed  Google Scholar 

  • 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–E2586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godde JS, Bickerton A (2006) The repetitive DNA elements called CRISPRs and their associated genes: evidence of horizontal transfer among prokaryotes. J Mol Evol 62:718–729

    Article  CAS  PubMed  Google Scholar 

  • Goldberg GW, Jiang W, Bikard D, Marraffini LA (2014) Conditional tolerance of temperate phages via transcription-dependent CRISPR-Cas targeting. Nature 514:633–637

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 8:172

    Article  CAS  Google Scholar 

  • Grogan DW (2003) Cytosine methylation by the SuaI restriction-modification system: implications for genetic fidelity in a hyperthermophilic archaeon. J Bacteriol 185:4657–4661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 108:9963–9968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 139:945–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 67:2746–2753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haurwitz RE, Jinek M, Wiedenheft B, Zhou K, Doudna JA (2010) Sequence- and structure-specific RNA processing by a CRISPR endonuclease. Science 329:1355–1358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He T, Li H, Zhang X (2017) Deep-sea hydrothermal vent viruses compensate for microbial metabolism in virus-host interactions. MBio 8:e00893

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 59:2695–2705

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hershey AD (1971) The bacteriophage lambda. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Hill C (1993) Bacteriophage and bacteriophage resistance in lactic acid bacteria. FEMS Microbiol Rev 12:87–108

    Article  CAS  Google Scholar 

  • 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 56:2255–2258

    CAS  PubMed  PubMed Central  Google Scholar 

  • Horvath P (2008) Diversity, activity, and evolution of CRISPR loci in Streptococcus thermophilus. J Bacteriol 190:1401

    Article  CAS  PubMed  Google Scholar 

  • Horvath P, Barrangou R (2010) CRISPR/Cas, the immune system of bacteria and archaea. Science 327:167–170

    Article  CAS  PubMed  Google Scholar 

  • Høyland-Kroghsbo NM, Mærkedahl RB, Svenningsen SL (2013) A quorum-sensing-induced bacteriophage defense mechanism. MBio 4:e00362–e00312

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Huang CX, Zhang YY, Jiao NZ (2010) Phage resistance of a marine bacterium, Roseobacter denitrificans OCh114, as revealed by comparative proteomics. Curr Microbiol 61:141–147

    Article  CAS  PubMed  Google Scholar 

  • Hur JK, Olovnikov I, Aravin AA (2014) Prokaryotic argonautes defend genomes against invasive DNA. Trends Biochem Sci 39:257–259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 63:3015–3020

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 169:5429–5433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jansen R, Embden JDV, Gaastra W, Schouls LM (2002a) Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43:1565–1575

    Article  CAS  PubMed  Google Scholar 

  • Jansen R, van Embden JD, Gaastra W, Schouls LM (2002b) Identification of a novel family of sequence repeats among prokaryotes. OMICS 6:23

    Article  CAS  PubMed  Google Scholar 

  • Jeffreys AJ, MacLeod A, Tamaki K, Neil DL, Monckton DG (1991) Minisatellite repeat coding as a digital approach to DNA typing. Nature 354:204–209

    Article  CAS  PubMed  Google Scholar 

  • Jiang W, Bikard D, Cox D, Zhang F, Marraffini LA (2013) RNA-guided editing of bacterial genomes using CRISPR-Cas systems. Nat Biotechnol 31:233–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 4:4823

    Article  PubMed  PubMed Central  Google Scholar 

  • Jin M, Xu C, Zhang X (2015) The effect of tryptophol on the bacteriophage infection in high-temperature environment. Appl Microbiol Biotechnol 99:8101–8111

    Article  CAS  PubMed  Google Scholar 

  • 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 337:816–821

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J (2013) RNA-programmed genome editing in human cells. elife 2:e00471

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 18:529–536

    Article  CAS  PubMed  Google Scholar 

  • Joung JK, Voytas DF, Kamens J (2015) Accelerating research through reagent repositories: the genome editing example. Genome Biol 16:255

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 170:2056–2062

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 188:15–22

    Article  CAS  PubMed  Google Scholar 

  • Kliem M, Dreiseikelmann B (1989) The superimmunity gene sim of bacteriophage P1 causes superinfection exclusion. Virology 171:350–355

    Article  CAS  PubMed  Google Scholar 

  • Koonin EV, Makarova KS, Wolf YI (2017) Evolutionary genomics of defense systems in archaea and bacteria. Annu Rev Microbiol 71:233–261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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–S88

    Article  CAS  PubMed  Google Scholar 

  • Krüger D, Bickle TA (1983) Bacteriophage survival: multiple mechanisms for avoiding the deoxyribonucleic acid restriction systems of their hosts. Microbiol Rev 47:345

    PubMed  PubMed Central  Google Scholar 

  • Krüger D, Barcak G, Smith H (1988) Abolition of DNA recognition site resistance to the restriction endonuclease EcoRII. Biomed Biochim Acta 47:K1–K5

    PubMed  Google Scholar 

  • Kunin V, Sorek R, Hugenholtz P (2007) Evolutionary conservation of sequence and secondary structures in CRISPR repeats. Genome Biol 8:R61

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Labrie SJ, Samson JE, Moineau S (2010) Bacteriophage resistance mechanisms. Nat Rev Microbiol 8:317–327

    Article  CAS  PubMed  Google Scholar 

  • 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 9:1383–1389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin LF, Posfai J, Roberts RJ, Kong H (2001) Comparative genomics of the restriction-modification systems in Helicobacter pylori. Proc Natl Acad Sci 98:2740–2745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindqvist BH, Deho G, Calendar R (1993) Mechanisms of genome propagation and helper exploitation by satellite phage P4. Microbiol Rev 57:683–702

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 29:527–543

    Article  CAS  PubMed  Google Scholar 

  • 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 53:163–166

    Article  CAS  PubMed  Google Scholar 

  • Loenen WA (2003) Tracking EcoKI and DNA fifty years on: a golden story full of surprises. Nucleic Acids Res 31:7059–7069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu MJ, Henning U (1994) Superinfection exclusion by T-even-type coliphages. Trends Microbiol 2:137–139

    Article  CAS  PubMed  Google Scholar 

  • Lu M, Stierhof Y, Henning U (1993) Location and unusual membrane topology of the immunity protein of the Escherichia coli phage T4. J Virol 67:4905–4913

    CAS  PubMed  PubMed Central  Google Scholar 

  • Magnuson R (2007) Hypothetical functions of toxin-antitoxin systems. J Bacteriol 189:6089–6092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mahony J, McGrath S, Fitzgerald GF, van Sinderen D (2008) Identification and characterization of lactococcal-prophage-carried superinfection exclusion genes. Appl Environ Microbiol 74:6206–6215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maillou J, Dreiseikelmann B (1990) The sim gene of Escherichia coli phage P1: nucleotide sequence and purification of the processed protein. Virology 175:500–507

    Article  CAS  PubMed  Google Scholar 

  • 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 189:5608–5616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 30:482–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Makarova KS, Wolf YI, Koonin EV (2013) Comparative genomics of defense systems in archaea and bacteria. Nucleic Acids Res 41:4360–4377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 9:467

    Article  CAS  PubMed  Google Scholar 

  • 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 13:722–736

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–1845

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 11:1029–1042

    Article  CAS  PubMed  Google Scholar 

  • Mathavan I, Beis K (2012) The role of bacterial membrane proteins in the internalization of microcin MccJ25 and MccB17. Portland Press Limited

    Google Scholar 

  • 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 69:277–282

    Article  CAS  Google Scholar 

  • Meyer JL, Huber JA (2014) Strain-level genomic variation in natural populations of Lebetimonas from an erupting deep-sea volcano. ISME J 8:867–880

    Article  CAS  PubMed  Google Scholar 

  • Moak M, Molineux IJ (2004) Peptidoglycan hydrolytic activities associated with bacteriophage virions. Mol Microbiol 51:1169–1183

    Article  CAS  PubMed  Google Scholar 

  • Mojica FJ, Juez G, Rodriguez-Valera F (1993) Transcription at different salinities of Haloferax mediterranei sequences adjacent to partially modified PstI sites. Mol Microbiol 9:613–621

    Article  CAS  PubMed  Google Scholar 

  • 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 17:85–93

    Article  CAS  PubMed  Google Scholar 

  • 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 36:244–246

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 64:3669–3673

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 65:64–71

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:171–179

    CAS  PubMed  Google Scholar 

  • Murray NE (2000) Type I restriction systems: sophisticated molecular machines (a legacy of Bertani and Weigle). Microbiol Mol Biol Rev 64:412–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakata A, Amemura M, Makino K (1989) Unusual nucleotide arrangement with repeated sequences in the Escherichia coli K-12 chromosome. J Bacteriol 171:3553–3556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 174:5719–5726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 20:5047–5052

    Article  PubMed  PubMed Central  Google Scholar 

  • Novick RP, Christie GE, Penades JR (2010) The phage-inducible chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8:541–551

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 65:330–335

    PubMed  PubMed Central  Google Scholar 

  • 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 36:866–875

    Article  PubMed  Google Scholar 

  • 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 6:497–510

    Article  CAS  PubMed  Google Scholar 

  • Penadés JR, Christie GE (2015) The phage-inducible chromosomal islands: a family of highly evolved molecular parasites. Annu Rev Virol 2:181–201

    Article  PubMed  CAS  Google Scholar 

  • Penadés JR, Chen J, Quiles-Puchalt N, Carpena N, Novick RP (2015) Bacteriophage-mediated spread of bacterial virulence genes. Curr Opin Microbiol 23:171–178

    Article  CAS  PubMed  Google Scholar 

  • Pingoud A (2012) Restriction endonucleases. Springer, Berlin

    Google Scholar 

  • Pingoud A, Fuxreiter M, Pingoud V, Wende W (2005) Type II restriction endonucleases: structure and mechanism. Cell Mol Life Sci 62:685

    Article  CAS  PubMed  Google Scholar 

  • 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 380:465–475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 5:274–284

    Article  PubMed  Google Scholar 

  • 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 91:423–437

    Article  CAS  Google Scholar 

  • 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 41:7260–7275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raleigh EA, Wilson G (1986) Escherichia coli K-12 restricts DNA containing 5-methylcytosine. Proc Natl Acad Sci 83:9070–9074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 109:16300–16305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 111:14536–14541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 375:720–734

    Article  CAS  PubMed  Google Scholar 

  • Ripp S, Miller RV (1998) Dynamics of the pseudolysogenic response in slowly growing cells of Pseudomonas aeruginosa. Microbiology 144:2225–2232

    Article  CAS  PubMed  Google Scholar 

  • 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 31:1805–1812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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–DD99

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 4:739

    Article  PubMed  Google Scholar 

  • 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 537:689–693

    Article  CAS  PubMed  Google Scholar 

  • Ruzin A, Lindsay J, Novick RP (2001) Molecular genetics of SaPI1-a mobile pathogenicity island in Staphylococcus aureus. Mol Microbiol 41:365–377

    Article  CAS  PubMed  Google Scholar 

  • Samson JE, Magadán AH, Sabri M, Moineau S (2013) Revenge of the phages: defeating bacterial defences. Nat Rev Microbiol 11:675

    Article  CAS  PubMed  Google Scholar 

  • Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32:347–355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 39:9275–9282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sashital DG, Wiedenheft B, Doudna JA (2012) Mechanism of foreign DNA selection in a bacterial adaptive immune system. Mol Cell 46:606–615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 143:509–516

    Article  CAS  PubMed  Google Scholar 

  • Schnabel H, Zillig W, Pfaffle M, Schnabel R, Michel H, Delius H (1982) Halobacterium halobium phage oH. EMBO J 1:87–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seed KD (2015) Battling phages: how bacteria defend against viral attack. PLoS Pathog 11:e1004847

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 23:720–723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 32:385–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Snyder L (1995) Phage-exclusion enzymes: a bonanza of biochemical and cell biology reagents? Mol Microbiol 15:415–420

    Article  CAS  PubMed  Google Scholar 

  • Snyder L, McWilliams K (1989) The rex genes of bacteriophage lambda can inhibit cell function without phage superinfection. Gene 81:17–24

    Article  CAS  PubMed  Google Scholar 

  • Sokolowski RD, Graham S, White MF (2014) Cas6 specificity and CRISPR RNA loading in a complex CRISPR-Cas system. Nucleic Acids Res 42:6532–6541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sorek R, Kunin V, Hugenholtz P (2008) CRISPR – a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6:181

    Article  CAS  PubMed  Google Scholar 

  • 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 405:863–876

    Article  CAS  PubMed  Google Scholar 

  • 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 56:518–530

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sternberg SH, Redding S, Jinek M, Greene EC, Doudna JA (2014) DNA interrogation by the CRISPR RNA-guided endonuclease Cas9. Nature 507:62–67

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stewart FJ, Panne D, Bickle TA, Raleigh EA (2000) Methyl-specific DNA binding by McrBC, a modification-dependent restriction enzyme 1. J Mol Biol 298:611–622

    Article  CAS  PubMed  Google Scholar 

  • Stirm S (1968) Escherichia coli K bacteriophages I. isolation and introductory characterization of five Escherichia coli K bacteriophages. J Virol 2:1107–1114

    CAS  PubMed  PubMed Central  Google Scholar 

  • Stoddard LI, Martiny JB, Marston MF (2007) Selection and characterization of cyanophage resistance in marine Synechococcus strains. Appl Environ Microbiol 73:5516–5522

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 350:146–157

    Article  CAS  PubMed  Google Scholar 

  • Sutherland IW (1995) Polysaccharide lyases. FEMS Microbiol Rev 16:323–347

    Article  CAS  PubMed  Google Scholar 

  • Suttle CA (2007) Marine viruses--major players in the global ecosystem. Nat Rev Microbiol 5:801–812

    Article  CAS  PubMed  Google Scholar 

  • Tallent SM, Christie GE (2007) Transducing particles of Staphylococcus aureus pathogenicity island SaPI1are comprised of helper phage-encoded proteins. J Bacteriol 189:7520–7524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 56:506–517

    Article  CAS  PubMed  Google Scholar 

  • Temple G, Ayling P, Wilkinson S (1986) Isolation and characterization of a lipopolysaccharide-specific bacteriophage of Pseudomonas aeruginosa. Microbios 45:81–91

    CAS  PubMed  Google Scholar 

  • Tock MR, Dryden DT (2005) The biology of restriction and anti-restriction. Curr Opin Microbiol 8:466–472

    Article  CAS  PubMed  Google Scholar 

  • 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 190:2434–2440

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 49:193–210

    Article  CAS  PubMed  Google Scholar 

  • 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 56:836–844

    Article  CAS  PubMed  Google Scholar 

  • 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 65:41–50

    Article  CAS  PubMed  Google Scholar 

  • 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 72:98–108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vasu K, Nagaraja V (2013) Diverse functions of restriction-modification systems in addition to cellular defense. Microbiol Mol Biol Rev 77:53–72

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vovis GF, Lacks S (1977) Complementary action of restriction enzymes endo R· DpnI and endo R· DpnII on bacteriophage f1 DNA. J Mol Biol 115:525–538

    Article  CAS  PubMed  Google Scholar 

  • Waldor MK, Mekalanos JJ (1996) Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272:1910–1914

    Article  CAS  PubMed  Google Scholar 

  • 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 9:187–194

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Zhang X (2010) Genome analysis of deep-sea thermophilic phage D6E. Appl Environ Microbiol 76:7861–7866

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 153:910–918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei D, Zhang X (2010) Proteomic analysis of interactions between a deep-sea thermophilic bacteriophage and its host at high temperature. J Virol 84:2365–2373

    Article  CAS  PubMed  Google Scholar 

  • Weinbauer MG (2004) Ecology of prokaryotic viruses. FEMS Microbiol Rev 28:127–181

    Article  CAS  PubMed  Google Scholar 

  • 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 108:10092–10097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 12:182–191

    Article  CAS  PubMed  Google Scholar 

  • 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 74:42–57

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wommack KE, Colwell RR (2000) Virioplankton: viruses in aquatic ecosystems. Microbiol Mol Biol Rev 64:69–114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 40:3610–3622

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Yamaguchi Y, Park JH, Inouye M (2011) Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 45:61–79

    Article  CAS  PubMed  Google Scholar 

  • 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 154:1370–1379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 176:5262–5269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Snyder L (1994) Translation elongation factor Tu cleaved by a phage-exclusion system. Proc Natl Acad Sci 91:802–806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zebec Z, Manica A, Zhang J, White MF, Schleper C (2014) CRISPR-mediated targeted mRNA degradation in the archaeon Sulfolobus solfataricus. Nucleic Acids Res 42:5280–5288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 191:210–219

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Jiao N (2009) Roseophage RDJLΦ1, infecting the aerobic anoxygenic phototrophic bacterium Roseobacter denitrificans OCh114. Appl Environ Microbiol 75:1745–1749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 191:2622–2629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Huang C, Yang J, Jiao N (2011) Interactions between marine microorganisms and their phages. Chin Sci Bull 56:1770

    Article  CAS  Google Scholar 

  • 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: 467

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xiaobo Zhang .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Jin, M., He, T., Zhang, X. (2019). Marine Microbe Stress Responses to Bacteriophage Infection. In: Zhang, X. (eds) Virus Infection and Tumorigenesis. Springer, Singapore. https://doi.org/10.1007/978-981-13-6198-2_5

Download citation

Publish with us

Policies and ethics