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A new perspective on lysogeny: prophages as active regulatory switches of bacteria

Nature Reviews Microbiology volume 13, pages 641–650 (2015)Cite this article

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Abstract

Unlike lytic phages, temperate phages that enter lysogeny maintain a long-term association with their bacterial host. In this context, mutually beneficial interactions can evolve that support efficient reproduction of both phages and bacteria. Temperate phages are integrated into the bacterial chromosome as large DNA insertions that can disrupt gene expression, and they may pose a fitness burden on the cell. However, they have also been shown to benefit their bacterial hosts by providing new functions in a bacterium–phage symbiotic interaction termed lysogenic conversion. In this Opinion article, we discuss another type of bacterium–phage interaction, active lysogeny, in which phages or phage-like elements are integrated into the bacterial chromosome within critical genes or operons and serve as switches that regulate bacterial genes via genome excision.

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Figure 1: The phage replication cycles.
Figure 2: Bacterium–phage lysogenic interactions.
Figure 3: Reversible active lysogeny regulates critical processes in bacteria.
Figure 4: Non-reversible active lysogeny regulates developmental processes in bacteria.

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References

  1. Twort, F. W. An investigation on the nature of ultra-microscopic viruses. Lancet 186, 1241–1243 (1915).

    Google Scholar 

  2. d'Herelle, F. An invisible microbe that is antagonistic to the dysentery Bacillus. Compt. Rend. Acad. Sci. Paris 165, 373–375 (1917).

    Google Scholar 

  3. Pawluk, A., Bondy-Denomy, J., Cheung, V. H., Maxwell, K. L. & Davidson, A. R. A new group of phage anti-CRISPR genes inhibits the type I-E CRISPR–Cas system of Pseudomonas aeruginosa. mBio 5, e00896 (2014).

    PubMed  PubMed Central  Google Scholar 

  4. Bobay, L. M., Touchon, M. & Rocha, E. P. Pervasive domestication of defective prophages by bacteria. Proc. Natl Acad. Sci. USA 111, 12127–12132 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Labrie, S. J., Samson, J. E. & Moineau, S. Bacteriophage resistance mechanisms. Nat. Rev. Microbiol. 8, 317–327 (2010).

    CAS  PubMed  Google Scholar 

  6. Stern, A. & Sorek, R. The phage-host arms race: shaping the evolution of microbes. Bioessays 33, 43–51 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Breitbart, M. & Rohwer, F. Here a virus, there a virus, everywhere the same virus? Trends Microbiol. 13, 278–284 (2005).

    CAS  PubMed  Google Scholar 

  8. Brussow, H. & Hendrix, R. W. Phage genomics: small is beautiful. Cell 108, 13–16 (2002).

    CAS  PubMed  Google Scholar 

  9. Ptashne, M. A Genetic Switch 3rd edn (CSHL Press, 2004).

    Google Scholar 

  10. Edlin, G., Lin, L. & Bitner, R. Reproductive fitness of P1, P2, and Mu lysogens of Escherichia coli. J. Virol. 21, 560–564 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Ravin, V. et al. Genomic sequence and analysis of the atypical temperate bacteriophage N15. J. Mol. Biol. 299, 53–73 (2000).

    CAS  PubMed  Google Scholar 

  12. Little, J. in Regulation of Gene Expression in Escherichia coli (eds Lin, E. C. C. & Lynch, A. S.) 453–479 (Springer US, 1996).

    Google Scholar 

  13. Lwoff, A. Lysogeny. Bacteriol. Rev. 17, 269–337 (1953).

    CAS  PubMed  PubMed Central  Google Scholar 

  14. Nanda, A. M., Thormann, K. & Frunzke, J. Impact of spontaneous prophage induction on the fitness of bacterial populations and host–microbe interactions. J. Bacteriol. 197, 410–419 (2015).

    PubMed  PubMed Central  Google Scholar 

  15. Nash, H. A. Integration and excision of bacteriophage λ: the mechanism of conservation site specific recombination. Annu. Rev. Genet. 15, 143–167 (1981).

    CAS  PubMed  Google Scholar 

  16. Shimada, K., Weisberg, R. A. & Gottesman, M. E. Prophage lambda at unusual chromosomal locations: I. Location of the secondary attachment sites and the properties of the lysogens. J. Mol. Biol. 63, 483–503 (1972).

    CAS  PubMed  Google Scholar 

  17. Harshey, R. M. The Mu story: how a maverick phage moved the field forward. Mob. DNA 3, 21 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Miller, R. V. & Ripp, S. A. in Horizontal Gene Transfer (eds Syvanen, M. & Kado, C. I.) 81–94 (Academic Press, 2001).

    Google Scholar 

  19. Baess, I. Report on a pseudolysogenic mycobacterium and a review of the literature concerning pseudolysogeny. Acta Pathol. Microbiol. Scand. B Microbiol. Immunol. 79, 428–434 (1971).

    CAS  PubMed  Google Scholar 

  20. Miller, R. & Day, M. in Bacteriophage Ecology (ed Abedon, S. T.) 114–144 (Cambridge Univ. Press, 2008).

    Google Scholar 

  21. Fuhrman, J. A. Marine viruses and their biogeochemical and ecological effects. Nature 399, 541–548 (1999).

    CAS  PubMed  Google Scholar 

  22. Suttle, C. A. & Chen, F. Mechanisms and rates of decay of marine viruses in seawater. Appl. Environ. Microbiol. 58, 3721–3729 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Hartley, M. A., Ronet, C. & Fasel, N. Backseat drivers: the hidden influence of microbial viruses on disease. Curr. Opin. Microbiol. 15, 538–545 (2012).

    PubMed  Google Scholar 

  24. Wagner, P. L. & Waldor, M. K. Bacteriophage control of bacterial virulence. Infect. Immun. 70, 3985–3993 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Brussow, H., Canchaya, C. & Hardt, W. D. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68, 560–602 (2004).

    PubMed  PubMed Central  Google Scholar 

  26. Casjens, S. Prophages and bacterial genomics: what have we learned so far? Mol. Microbiol. 49, 277–300 (2003).

    CAS  PubMed  Google Scholar 

  27. Frobisher, M. & Brown, J. Transmissible toxicogenicity of Streptococci. Bull. Johns Hopkins Hosp. 41, 167–173 (1927).

    Google Scholar 

  28. Freeman, V. J. Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. J. Bacteriol. 61, 675–688 (1951).

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Fujii, N., Oguma, K., Yokosawa, N., Kimura, K. & Tsuzuki, K. Characterization of bacteriophage nucleic acids obtained from Clostridium botulinum types C and D. Appl. Environ. Microbiol. 54, 69–73 (1988).

    CAS  PubMed  PubMed Central  Google Scholar 

  30. Barksdale, L. & Arden, S. B. Persisting bacteriophage infections, lysogeny, and phage conversions. Annu. Rev. Microbiol. 28, 265–299 (1974).

    CAS  PubMed  Google Scholar 

  31. Plunkett, G. 3rd, Rose, D. J., Durfee, T. J. & Blattner, F. R. Sequence of Shiga toxin 2 phage 933W from Escherichia coli O157:H7: Shiga toxin as a phage late-gene product. J. Bacteriol. 181, 1767–1778 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Waldor, M. K. & Mekalanos, J. J. Lysogenic conversion by a filamentous phage encoding cholera toxin. Science 272, 1910–1914 (1996).

    CAS  PubMed  Google Scholar 

  33. Faruque, S. M., Albert, M. J. & Mekalanos, J. J. Epidemiology, genetics, and ecology of toxigenic Vibrio cholerae. Microbiol. Mol. Biol. Rev. 62, 1301–1314 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Mirold, S. et al. Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc. Natl Acad. Sci. USA 96, 9845–9850 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Coleman, D. C. et al. Staphylococcus aureus bacteriophages mediating the simultaneous lysogenic conversion of β-lysin, staphylokinase and enterotoxin A: molecular mechanism of triple conversion. J. Gen. Microbiol. 135, 1679–1697 (1989).

    CAS  PubMed  Google Scholar 

  36. Muhldorfer, I. et al. Regulation of the Shiga-like toxin II operon in Escherichia coli. Infect. Immun. 64, 495–502 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  37. Wagner, P. L. et al. Role for a phage promoter in Shiga toxin 2 expression from a pathogenic Escherichia coli strain. J. Bacteriol. 183, 2081–2085 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Livny, J. & Friedman, D. I. Characterizing spontaneous induction of Stx encoding phages using a selectable reporter system. Mol. Microbiol. 51, 1691–1704 (2004).

    CAS  PubMed  Google Scholar 

  39. Reidl, J. & Klose, K. E. Vibrio cholerae and cholera: out of the water and into the host. FEMS Microbiol. Rev. 26, 125–139 (2002).

    CAS  PubMed  Google Scholar 

  40. de Kievit, T. R. & Iglewski, B. H. Bacterial quorum sensing in pathogenic relationships. Infect. Immun. 68, 4839–4849 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Dunny, G. M. & Leonard, B. A. Cell–cell communication in Gram-positive bacteria. Annu. Rev. Microbiol. 51, 527–564 (1997).

    CAS  PubMed  Google Scholar 

  42. Waldor, M. K. & Friedman, D. I. Phage regulatory circuits and virulence gene expression. Curr. Opin. Microbiol. 8, 459–465 (2005).

    CAS  PubMed  Google Scholar 

  43. Casas, V. & Maloy, S. Role of bacteriophage-encoded exotoxins in the evolution of bacterial pathogens. Future Microbiol. 6, 1461–1473 (2011).

    CAS  PubMed  Google Scholar 

  44. McShan, W. M., Tang, Y. F. & Ferretti, J. J. Bacteriophage T12 of Streptococcus pyogenes integrates into the gene encoding a serine tRNA. Mol. Microbiol. 23, 719–728 (1997).

    CAS  PubMed  Google Scholar 

  45. Williams, K. P. Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res. 30, 866–875 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Dubnau, D. DNA uptake in bacteria. Annu. Rev. Microbiol. 53, 217–244 (1999).

    CAS  PubMed  Google Scholar 

  47. Grossman, A. D. Genetic networks controlling the initiation of sporulation and the development of genetic competence in Bacillus subtilis. Annu. Rev. Genet. 29, 477–508 (1995).

    CAS  PubMed  Google Scholar 

  48. Claverys, J. P., Prudhomme, M. & Martin, B. Induction of competence regulons as a general response to stress in Gram-positive bacteria. Annu. Rev. Microbiol. 60, 451–475 (2006).

    CAS  PubMed  Google Scholar 

  49. Borezee, E., Msadek, T., Durant, L. & Berche, P. Identification in Listeria monocytogenes of MecA, a homologue of the Bacillus subtilis competence regulatory protein. J. Bacteriol. 182, 5931–5934 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Loessner, M. J., Inman, R. B., Lauer, P. & Calendar, R. Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution. Mol. Microbiol. 35, 324–340 (2000).

    CAS  PubMed  Google Scholar 

  51. Klumpp, J. & Loessner, M. J. Listeria phages: genomes, evolution, and application. Bacteriophage 3, e26861 (2013).

    PubMed  PubMed Central  Google Scholar 

  52. Zink, R. & Loessner, M. J. Classification of virulent and temperate bacteriophages of Listeria spp. on the basis of morphology and protein analysis. Appl. Environ. Microbiol. 58, 296–302 (1992).

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Loessner, M. J., Wendlinger, G. & Scherer, S. Heterogeneous endolysins in Listeria monocytogenes bacteriophages: a new class of enzymes and evidence for conserved holin genes within the siphoviral lysis cassettes. Mol. Microbiol. 16, 1231–1241 (1995).

    CAS  PubMed  Google Scholar 

  54. Rabinovich, L., Sigal, N., Borovok, I., Nir-Paz, R. & Herskovits, A. A. Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence. Cell 150, 792–802 (2012).

    CAS  PubMed  Google Scholar 

  55. Hamon, M., Bierne, H. & Cossart, P. Listeria monocytogenes: a multifaceted model. Nat. Rev. Microbiol. 4, 423–434 (2006).

    CAS  PubMed  Google Scholar 

  56. Rosenberg, S. M. Evolving responsively: adaptive mutation. Nat. Rev. Genet. 2, 504–515 (2001).

    CAS  PubMed  Google Scholar 

  57. LeClerc, J. E., Li, B., Payne, W. L. & Cebula, T. A. High mutation frequencies among Escherichia coli and Salmonella pathogens. Science 274, 1208–1211 (1996).

    CAS  PubMed  Google Scholar 

  58. Jolivet-Gougeon, A. et al. Bacterial hypermutation: clinical implications. J. Med. Microbiol. 60, 563–573 (2011).

    CAS  PubMed  Google Scholar 

  59. Scott, J., Nguyen, S. V., King, C. J., Hendrickson, C. & McShan, W. M. Phage-like Streptococcus pyogenes chromosomal islands (SpyCI) and mutator phenotypes: control by growth state and rescue by a SpyCI-encoded promoter. Front. Microbiol. 3, 317 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Novick, R. P., Christie, G. E. & Penades, J. R. The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 8, 541–551 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  61. Scott, J., Thompson-Mayberry, P., Lahmamsi, S., King, C. J. & McShan, W. M. Phage-associated mutator phenotype in group A Streptococcus. J. Bacteriol. 190, 6290–6301 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  62. Canchaya, C. et al. Genome analysis of an inducible prophage and prophage remnants integrated in the Streptococcus pyogenes strain SF370. Virology 302, 245–258 (2002).

    CAS  PubMed  Google Scholar 

  63. Nguyen, S. V. & McShan, W. M. Chromosomal islands of Streptococcus pyogenes and related streptococci: molecular switches for survival and virulence. Front. Cell. Infect. Microbiol. 4, 109 (2014).

    PubMed  PubMed Central  Google Scholar 

  64. Kimura, T., Amaya, Y., Kobayashi, K., Ogasawara, N. & Sato, T. Repression of sigK intervening (skin) element gene expression by the CI-like protein SknR and effect of SknR depletion on growth of Bacillus subtilis cells. J. Bacteriol. 192, 6209–6216 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Stragier, P., Kunkel, B., Kroos, L. & Losick, R. Chromosomal rearrangement generating a composite gene for a developmental transcription factor. Science 243, 507–512 (1989).

    CAS  PubMed  Google Scholar 

  66. Kunkel, B., Losick, R. & Stragier, P. The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene. Genes Dev. 4, 525–535 (1990).

    CAS  PubMed  Google Scholar 

  67. Takemaru, K., Mizuno, M., Sato, T., Takeuchi, M. & Kobayashi, Y. Complete nucleotide sequence of a skin element excised by DNA rearrangement during sporulation in Bacillus subtilis. Microbiology 141, 323–327 (1995).

    CAS  PubMed  Google Scholar 

  68. Sato, T. & Kobayashi, Y. The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J. Bacteriol. 180, 1655–1661 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Silvaggi, J. M., Perkins, J. B. & Losick, R. Small untranslated RNA antitoxin in Bacillus subtilis. J. Bacteriol. 187, 6641–6650 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Yamaguchi, Y., Park, J. H. & Inouye, M. Toxin-antitoxin systems in bacteria and archaea. Annu. Rev. Genet. 45, 61–79 (2011).

    CAS  PubMed  Google Scholar 

  71. Hayes, F. & Kedzierska, B. Regulating toxin-antitoxin expression: controlled detonation of intracellular molecular timebombs. Toxins (Basel) 6, 337–358 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  72. Eichenberger, P. et al. The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis. PLoS Biol. 2, e328 (2004).

    PubMed  PubMed Central  Google Scholar 

  73. Errington, J. Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Microbiol. Rev. 57, 1–33 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Sato, T., Harada, K. & Kobayashi, Y. Analysis of suppressor mutations of spoIVCA mutations: occurrence of DNA rearrangement in the absence of site-specific DNA recombinase SpoIVCA in Bacillus subtilis. J. Bacteriol. 178, 3380–3383 (1996).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Kim, K. P. et al. Inducible Clostridium perfringens bacteriophages ΦS9 and ΦS63: different genome structures and a fully functional sigK intervening element. Bacteriophage 2, 89–97 (2012).

    PubMed  PubMed Central  Google Scholar 

  76. Abe, K. et al. Regulated DNA rearrangement during sporulation in Bacillus weihenstephanensis KBAB4. Mol. Microbiol. 90, 415–427 (2013).

    CAS  PubMed  Google Scholar 

  77. Abe, K. et al. Developmentally-regulated excision of the SPβ prophage reconstitutes a gene required for spore envelope maturation in Bacillus subtilis. PLoS Genet. 10, e1004636 (2014).

    PubMed  PubMed Central  Google Scholar 

  78. Kumar, K., Mella-Herrera, R. A. & Golden, J. W. Cyanobacterial heterocysts. Cold Spring Harb. Perspect. Biol. 2, a000315 (2010).

    PubMed  PubMed Central  Google Scholar 

  79. Carrasco, C. D., Holliday, S. D., Hansel, A., Lindblad, P. & Golden, J. W. Heterocyst-specific excision of the Anabaena sp. strain PCC 7120 hupL element requires xisC. J. Bacteriol. 187, 6031–6038 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  80. Henson, B. J., Hartman, L., Watson, L. E. & Barnum, S. R. Evolution and variation of the nifD and hupL elements in the heterocystous cyanobacteria. Int. J. Syst. Evol. Microbiol. 61, 2938–2949 (2011).

    CAS  PubMed  Google Scholar 

  81. Golden, J. W., Robinson, S. J. & Haselkorn, R. Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena. Nature 314, 419–423 (1985).

    CAS  PubMed  Google Scholar 

  82. Carrasco, C. D., Buettner, J. A. & Golden, J. W. Programmed DNA rearrangement of a cyanobacterial hupL gene in heterocysts. Proc. Natl Acad. Sci. USA 92, 791–795 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  83. Thanassi, J. A., Hartman-Neumann, S. L., Dougherty, T. J., Dougherty, B. A. & Pucci, M. J. Identification of 113 conserved essential genes using a high-throughput gene disruption system in Streptococcus pneumoniae. Nucleic Acids Res. 30, 3152–3162 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Stewart, F. M. & Levin, B. R. The population biology of bacterial viruses: why be temperate. Theor. Popul. Biol. 26, 93–117 (1984).

    CAS  PubMed  Google Scholar 

  85. Campbell, A. Conditions for the existence of bacteriophage. Evolution 15, 153–165 (1961).

    Google Scholar 

  86. Edlin, G., Lin, L. & Kudrna, R. λ lysogens of E. coli reproduce more rapidly than non-lysogens. Nature 255, 735–737 (1975).

    CAS  PubMed  Google Scholar 

  87. Lin, L., Bitner, R. & Edlin, G. Increased reproductive fitness of Escherichia coli lambda lysogens. J. Virol. 21, 554–559 (1977).

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Herron-Olson, L., Fitzgerald, J. R., Musser, J. M. & Kapur, V. Molecular correlates of host specialization in Staphylococcus aureus. PLoS ONE 2, e1120 (2007).

    PubMed  PubMed Central  Google Scholar 

  89. Lowder, B. V. et al. Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc. Natl Acad. Sci. USA 106, 19545–19550 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Goerke, C., Wirtz, C., Fluckiger, U. & Wolz, C. Extensive phage dynamics in Staphylococcus aureus contributes to adaptation to the human host during infection. Mol. Microbiol. 61, 1673–1685 (2006).

    CAS  PubMed  Google Scholar 

  91. Utter, B. et al. Beyond the chromosome: the prevalence of unique extra-chromosomal bacteriophages with integrated virulence genes in pathogenic Staphylococcus aureus. PLoS ONE 9, e100502 (2014).

    PubMed  PubMed Central  Google Scholar 

  92. Salgado-Pabon, W. et al. Staphylococcus aureus β-toxin production is common in strains with the β-toxin gene inactivated by bacteriophage. J. Infect. Dis. 210, 784–792 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Bae, T., Baba, T., Hiramatsu, K. & Schneewind, O. Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol. Microbiol. 62, 1035–1047 (2006).

    CAS  PubMed  Google Scholar 

  94. Luneberg, E. et al. Phase-variable expression of lipopolysaccharide contributes to the virulence of Legionella pneumophila. J. Exp. Med. 188, 49–60 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  95. Luneberg, E. et al. Chromosomal insertion and excision of a 30 kb unstable genetic element is responsible for phase variation of lipopolysaccharide and other virulence determinants in Legionella pneumophila. Mol. Microbiol. 39, 1259–1271 (2001).

    CAS  PubMed  Google Scholar 

  96. Mah, T. F. & O'Toole, G. A. Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol. 9, 34–39 (2001).

    CAS  PubMed  Google Scholar 

  97. O'Toole, G. A. & Kolter, R. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol. Microbiol. 30, 295–304 (1998).

    CAS  PubMed  Google Scholar 

  98. Kirby, J. E., Trempy, J. E. & Gottesman, S. Excision of a P4-like cryptic prophage leads to Alp protease expression in Escherichia coli. J. Bacteriol. 176, 2068–2081 (1994).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Wang, X., Kim, Y. & Wood, T. K. Control and benefits of CP4-57 prophage excision in Escherichia coli biofilms. ISME J. 3, 1164–1179 (2009).

    CAS  PubMed  Google Scholar 

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Acknowledgements

The research in the Herskovits laboratory is funded by a European Research Council (ERC) starting grant (PathoPhageHost) and Infect-ERA grant (PROANTILIS) of the ERC-FP7 programme.

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  1. Ron Feiner and Tal Argov: R.F. and T.A. contributed equally to this work.

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  1. Ilya Borovok and Anat A. Herskovits are at the Department of Molecular Microbiology and Biotechnology, Ron Feiner, Tal Argov, Lev Rabinovich, Nadejda Sigal, Tel Aviv University, Tel Aviv 69978, Israel.,

    Ron Feiner, Tal Argov, Lev Rabinovich, Nadejda Sigal, Ilya Borovok & Anat A. Herskovits

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Feiner, R., Argov, T., Rabinovich, L. et al. A new perspective on lysogeny: prophages as active regulatory switches of bacteria. Nat Rev Microbiol 13, 641–650 (2015). https://doi.org/10.1038/nrmicro3527

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