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Annual Review of Virology

Volume 2, 2015

The Phage-Inducible Chromosomal Islands: A Family of Highly Evolved Molecular Parasites

Abstract

The phage-inducible chromosomal islands (PICIs) are a family of highly mobile genetic elements that contribute substantively to horizontal gene transfer, host adaptation, and virulence. Initially identified in , these elements are now thought to occur widely in gram-positive bacteria. They are molecular parasites that exploit certain temperate phages as helpers, using a variety of elegant strategies to manipulate the phage life cycle and promote their own spread, both intra- and intergenerically. At the same time, these PICI-encoded mechanisms severely interfere with helper phage reproduction, thereby enhancing survival of the bacterial population. In this review we discuss the genetics and the life cycle of these elements, with special emphasis on how they interact and interfere with the helper phage machinery for their own benefit. We also analyze the role that these elements play in driving bacterial and viral evolution.

Keyword(s): bacteriophage, evolution, horizontal gene transfer, molecular piracy, pathogenicity island, virulence
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2015-11-09
2024-04-19
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Literature Cited

  1. Freeman VJ. 1.  1951. Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. J. Bacteriol. 61:675–88 [Google Scholar]
  2. Wagner PL, Waldor MK. 2.  2002. Bacteriophage control of bacterial virulence. Infect. Immun. 70:3985–93 [Google Scholar]
  3. Boyd EF. 3.  2012. Bacteriophage-encoded bacterial virulence factors and phage–pathogenicity island interactions. Adv. Virus Res. 82:91–118 [Google Scholar]
  4. Brüssow H, Canchaya C, Hardt WD. 4.  2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68:560–602 [Google Scholar]
  5. Fortier LC, Sekulovic O. 5.  2013. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4:354–65 [Google Scholar]
  6. Penadés JR, Chen J, Quiles-Puchalt N, Carpena N, Novick RP. 6.  2015. Bacteriophage-mediated spread of bacterial virulence genes. Curr. Opin. Microbiol. 23:171–78 [Google Scholar]
  7. Sandri RM, Berger H. 7.  1980. Bacteriophage P1-mediated generalized transduction in Escherichia coli: fate of transduced DNA in rec+ and recA− recipients. Virology 106:14–29 [Google Scholar]
  8. Ebel-Tsipis J, Botstein D, Fox MS. 8.  1972. Generalized transduction by phage P22 in Salmonella typhimurium. I. Molecular origin of transducing DNA. J. Mol. Biol. 71:433–48 [Google Scholar]
  9. Ikeda H, Tomizawa JI. 9.  1965. Transducing fragments in generalized transduction by phage P1. I. Molecular origin of the fragments. J. Mol. Biol. 14:85–109 [Google Scholar]
  10. Bergdoll MS, Crass BA, Reiser RF, Robbins RN, Davis JP. 10.  1981. A new staphylococcal enterotoxin, enterotoxin F, associated with toxic-shock-syndrome Staphylococcus aureus isolates. Lancet 1:1017–21 [Google Scholar]
  11. Schutzer SE, Fischetti VA, Zabriskie JB. 11.  1983. Toxic shock syndrome and lysogeny in Staphylococcus aureus. Science 220:316–18 [Google Scholar]
  12. Kreiswirth BN, Löfdahl S, Betley MJ, O'Reilly M, Schlievert PM. 12.  et al. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709–12 [Google Scholar]
  13. Chu MC, Kreiswirth BN, Pattee PA, Novick RP, Melish ME, James JF. 13.  1988. Association of toxic shock toxin-1 determinant with a heterologous insertion at multiple loci in the Staphylococcus aureus chromosome. Infect. Immun. 56:2702–8 [Google Scholar]
  14. Lindsay JA, Ruzin A, Ross HF, Kurepina N, Novick RP. 14.  1998. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol. Microbiol. 29:527–43The original report describing the biology of SaPIs. [Google Scholar]
  15. Ruzin A, Lindsay J, Novick RP. 15.  2001. Molecular genetics of SaPI1—a mobile pathogenicity island in Staphylococcus aureus. Mol. Microbiol. 41:365–77 [Google Scholar]
  16. Fitzgerald JR, Monday SR, Foster TJ, Bohach GA, Hartigan PJ. 16.  et al. 2001. Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J. Bacteriol. 183:63–70 [Google Scholar]
  17. Úbeda C, Tormo MÁ, Cucarella C, Trotonda P, Foster TJ. 17.  et al. 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 [Google Scholar]
  18. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penadés JR. 18.  2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183:2888–96 [Google Scholar]
  19. Úbeda C, Maiques E, Knecht E, Lasa I, Novick RP, Penadés JR. 19.  2005. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol. Microbiol. 56:836–44 [Google Scholar]
  20. Novick RP, Christie GE, Penadés JR. 20.  2010. The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 8:541–51 [Google Scholar]
  21. Lindqvist BH, Dehò G, Calendar R. 21.  1993. Mechanisms of genome propagation and helper exploitation by satellite phage P4. Microbiol. Rev. 57:683–702 [Google Scholar]
  22. Arnold HP, She Q, Phan H, Stedman K, Prangishvili D. 22.  et al. 1999. The genetic element pSSVx of the extremely thermophilic crenarchaeon Sulfolobus is a hybrid between a plasmid and a virus. Mol. Microbiol. 34:217–26 [Google Scholar]
  23. Maiques E, Úbeda C, Campoy S, Salvador N, Lasa I. 23.  et al. 2006. β-Lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J. Bacteriol. 188:2726–29 [Google Scholar]
  24. Selva L, Viana D, Regev-Yochay G, Trzcinski K, Corpa JM. 24.  et al. 2009. Killing niche competitors by remote-control bacteriophage induction. PNAS 106:1234–38 [Google Scholar]
  25. Chen J, Novick RP. 25.  2009. Phage-mediated intergeneric transfer of toxin genes. Science 323:139–41The first demonstration of intergeneric transfer of SaPIs. [Google Scholar]
  26. Maiques E, Úbeda C, Tormo MÁ, Ferrer MD, Lasa I. 26.  et al. 2007. Role of staphylococcal phage and SaPI integrase in intra- and interspecies SaPI transfer. J. Bacteriol. 189:5608–16 [Google Scholar]
  27. Chen J, Carpena N, Quiles-Puchalt N, Ram G, Novick RP, Penadés JR. 27.  2014. Intra- and inter-generic transfer of pathogenicity island-encoded virulence genes by cos phages. ISME J. 9:1260–63 [Google Scholar]
  28. Winstel V, Liang C, Sanchez-Carballo P, Steglich M, Munar M. 28.  et al. 2013. Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens. Nat. Commun. 4:2345 [Google Scholar]
  29. Tormo-Más MÁ, Mir I, Shrestha A, Tallent SM, Campoy S. 29.  et al. 2010. Moonlighting bacteriophage proteins derepress staphylococcal pathogenicity islands. Nature 465:779–82Elucidation of the mechanism of SaPI induction by phage-encoded antirepressors. [Google Scholar]
  30. Úbeda C, Maiques E, Barry P, Matthews A, Tormo MÁ. 30.  et al. 2008. SaPI mutations affecting replication and transfer and enabling autonomous replication in the absence of helper phage. Mol. Microbiol. 67:493–503 [Google Scholar]
  31. Lane KD. 31.  2013. Transcriptional crosstalk between helper bacteriophages and Staphylococcus aureus pathogenicity islands. PhD Diss., Va. Commonw. Univ., Richmond
  32. Campbell A. 32.  2007. Phage integration and chromosome structure. A personal history. Annu. Rev. Genet. 41:1–11 [Google Scholar]
  33. Subedi A, Úbeda C, Adhikari RP, Penadés JR, Novick RP. 33.  2007. Sequence analysis reveals genetic exchanges and intraspecific spread of SaPI2, a pathogenicity island involved in menstrual toxic shock. Microbiology 153:3235–45 [Google Scholar]
  34. Mir-Sanchis I, Martínez-Rubio R, Martí M, Chen J, Lasa I. 34.  et al. 2012. Control of Staphylococcus aureus pathogenicity island excision. Mol. Microbiol. 85:833–45 [Google Scholar]
  35. Úbeda C, Barry P, Penadés JR, Novick RP. 35.  2007. A pathogenicity island replicon in Staphylococcus aureus replicates as an unstable plasmid. PNAS 104:14182–88 [Google Scholar]
  36. Úbeda C, Tormo-Más MÁ, Penadés JR, Novick RP. 36.  2012. Structure-function analysis of the SaPIbov1 replication origin in Staphylococcus aureus. Plasmid 67:183–90 [Google Scholar]
  37. Úbeda C, Maiques E, Tormo MÁ, Campoy S, Lasa I. 37.  et al. 2007. SaPI operon I is required for SaPI packaging and is controlled by LexA. Mol. Microbiol. 65:41–50SaPI operon I is required for SaPI packaging and is controlled by LexA. The first genetic analysis of SaPI genes involved in helper exploitation. [Google Scholar]
  38. Bento JC, Lane KD, Read EK, Cerca N, Christie GE. 38.  2014. Sequence determinants for DNA packaging specificity in the Staphylococcus aureus pathogenicity island SaPI1. Plasmid 71:8–15 [Google Scholar]
  39. Chen J, Ram G, Penadés JR, Brown S, Novick RP. 39.  2015. Pathogenicity island-directed transfer of unlinked chromosomal virulence genes. Mol. Cell 57:138–49Demonstration of SaPI-directed transfer of chromosomal virulence genes. [Google Scholar]
  40. Ram G, Chen J, Kumar K, Ross HF, Úbeda C. 40.  et al. 2012. Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism. PNAS 109:16300–5Characterization of the first SaPI gene responsible for inhibition of phage packaging. [Google Scholar]
  41. Poliakov A, Chang JR, Spilman MS, Damle PK, Christie GE. 41.  et al. 2008. Capsid size determination by Staphylococcus aureus pathogenicity island SaPI1 involves specific incorporation of SaPI1 proteins into procapsids. J. Mol. Biol. 380:465–75 [Google Scholar]
  42. Úbeda C, Olivarez NP, Barry P, Wang H, Kong X. 42.  et al. 2009. Specificity of staphylococcal phage and SaPI DNA packaging as revealed by integrase and terminase mutations. Mol. Microbiol. 72:98–108 [Google Scholar]
  43. Ram G, Chen J, Ross HF, Novick RP. 43.  2014. Precisely modulated pathogenicity island interference with late phage gene transcription. PNAS 111:14536–41Elucidation of SaPI interference with helper phage late transcription. [Google Scholar]
  44. Harwich MD. 44.  2009. Transcriptional profiling of staphylococcal bacteriophage 80α and regulatory interactions with pathogenicity island SaPI1 PhD Diss., Virginia Commonw. Univ., Richmond
  45. Malachowa N, DeLeo FR. 45.  2010. Mobile genetic elements of Staphylococcus aureus. Cell. Mol. Life Sci. 67:3057–71 [Google Scholar]
  46. Viana D, Blanco J, Tormo-Más MÁ, Selva L, Guinane CM. 46.  et al. 2010. Adaptation of Staphylococcus aureus to ruminant and equine hosts involves SaPI-carried variants of von Willebrand factor-binding protein. Mol. Microbiol. 77:1583–94 [Google Scholar]
  47. Guinane CM, Ben Zakour NL, Tormo-Más MÁ, Weinert LA, Lowder BV. 47.  et al. 2010. Evolutionary genomics of Staphylococcus aureus reveals insights into the origin and molecular basis of ruminant host adaptation. Genome Biol. Evol. 2:454–66 [Google Scholar]
  48. O'Neill AJ, Larsen AR, Skov R, Henriksen AS, Chopra I. 48.  2007. Characterization of the epidemic European fusidic acid-resistant impetigo clone of Staphylococcus aureus. J. Clin. Microbiol. 45:1505–10 [Google Scholar]
  49. Chen HJ, Chang YC, Tsai JC, Hung WC, Lin YT. 49.  et al. 2013. New structure of phage-related islands carrying fusB and a virulence gene in fusidic acid-resistant Staphylococcus epidermidis. Antimicrob. Agents Chemother. 57:5737–39 [Google Scholar]
  50. Kuroda M, Yamashita A, Hirakawa H, Kumano M, Morikawa K. 50.  et al. 2005. Whole genome sequence of Staphylococcus saprophyticus reveals the pathogenesis of uncomplicated urinary tract infection. PNAS 102:13272–77 [Google Scholar]
  51. Christie GE, Dokland T. 51.  2012. Pirates of the Caudovirales. Virology 434:210–21 [Google Scholar]
  52. Damle PK, Wall EA, Spilman MS, Dearborn AD, Ram G. 52.  et al. 2012. The roles of SaPI1 proteins gp7 (CpmA) and gp6 (CpmB) in capsid size determination and helper phage interference. Virology 432:277–82Contributions of the SaPI-encoded capsid morphogenesis proteins to virion assembly and size. [Google Scholar]
  53. Tormo-Más MÁ, Donderis J, García-Caballer M, Alt A, Mir-Sanchis I. 53.  et al. 2013. Phage dUTPases control transfer of virulence genes by a proto-oncogenic G protein-like mechanism. Mol. Cell 49:947–58 [Google Scholar]
  54. Tallent SM, Christie GE. 54.  2007. Transducing particles of Staphylococcus aureus pathogenicity island SaPI1 are comprised of helper phage-encoded proteins. J. Bacteriol. 189:7520–24 [Google Scholar]
  55. Tormo MÁ, Ferrer MD, Maiques E, Úbeda C, Selva L. 55.  et al. 2008. Staphylococcus aureus pathogenicity island DNA is packaged in particles composed of phage proteins. J. Bacteriol. 190:2434–40 [Google Scholar]
  56. Quiles-Puchalt N, Carpena N, Alonso JC, Novick RP, Marina A, Penadés JR. 56.  2014. Staphylococcal pathogenicity island DNA packaging system involving cos-site packaging and phage-encoded HNH endonucleases. PNAS 111:6016–21SaPI transfer by cos phages and a novel packaging system involving HNH endonucleases. [Google Scholar]
  57. Dearborn AD, Dokland T. 57.  2012. Mobilization of pathogenicity islands by Staphylococcus aureus strain Newman bacteriophages. Bacteriophage 2:70–78 [Google Scholar]
  58. Liu J, Dehbi M, Moeck G, Arhin F, Bauda P. 58.  et al. 2004. Antimicrobial drug discovery through bacteriophage genomics. Nat. Biotechnol. 22:185–91 [Google Scholar]
  59. Spilman MS, Dearborn AD, Chang JR, Damle PK, Christie GE, Dokland T. 59.  2011. A conformational switch involved in maturation of Staphylococcus aureus bacteriophage 80α capsids. J. Mol. Biol. 405:863–76 [Google Scholar]
  60. Quiles-Puchalt N, Martínez-Rubio R, Ram G, Lasa I, Penadés JR. 60.  2014. Unravelling bacteriophage φ11 requirements for packaging and transfer of mobile genetic elements in Staphylococcus aureus. Mol. Microbiol. 91:423–37 [Google Scholar]
  61. Dearborn AD, Spilman MS, Damle PK, Chang JR, Monroe EB. 61.  et al. 2011. The Staphylococcus aureus pathogenicity island 1 protein gp6 functions as an internal scaffold during capsid size determination. J. Mol. Biol. 412:710–22 [Google Scholar]
  62. Spilman MS, Damle PK, Dearborn AD, Rodenburg CM, Chang JR. 62.  et al. 2012. Assembly of bacteriophage 80α capsids in a Staphylococcus aureus expression system. Virology 434:242–50 [Google Scholar]
  63. Christie GE, Matthews AM, King DG, Lane KD, Olivarez NP. 63.  et al. 2010. The complete genomes of Staphylococcus aureus bacteriophages 80 and 80α—implications for the specificity of SaPI mobilization. Virology 407:381–90 [Google Scholar]
  64. Feiss M, Rao VB. 64.  2012. The bacteriophage DNA packaging machine. Adv. Exp. Med. Biol. 726:489–509 [Google Scholar]
  65. Quiles-Puchalt N, Tormo-Más MÁ, Campoy S, Toledo-Arana A, Monedero V. 65.  et al. 2013. A super-family of transcriptional activators regulates bacteriophage packaging and lysis in Gram-positive bacteria. Nucleic Acids Res. 41:7260–75 [Google Scholar]
  66. Ferrer MD, Quiles-Puchalt N, Harwich MD, Tormo-Más MÁ, Campoy S. 66.  et al. 2011. RinA controls phage-mediated packaging and transfer of virulence genes in Gram-positive bacteria. Nucleic Acids Res. 39:5866–78 [Google Scholar]
  67. Duerkop BA, Clements CV, Rollins D, Rodrigues JLM, Hooper LV. 67.  2012. A composite bacteriophage alters colonization by an intestinal commensal bacterium. PNAS 109:17621–26 [Google Scholar]
  68. Matos RC, Lapaque N, Rigottier-Gois L, Debarbieux L, Meylheuc T. 68.  et al. 2013. Enterococcus faecalis prophage dynamics and contributions to pathogenic traits. PLOS Genet. 9:e1003539First report of a bona fide non-SaPI PICI element (in E. faecalis). [Google Scholar]
  69. Scott J, Thompson-Mayberry P, Lahmamsi S, King CJ, McShan WM. 69.  2008. Phage-associated mutator phenotype in group A streptococcus. J. Bacteriol. 190:6290–301 [Google Scholar]
  70. Scott J, Nguyen SV, King CJ, Hendrickson C, McShan WM. 70.  2012. 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 [Google Scholar]
  71. Nguyen SV, McShan WM. 71.  2014. Chromosomal islands of Streptococcus pyogenes and related streptococci: molecular switches for survival and virulence. Front. Cell. Infect. Microbiol. 4:109 [Google Scholar]
  72. Croucher NJ, Coupland PG, Stevenson AE, Callendrello A, Bentley SD, Hanage WP. 72.  2014. Diversification of bacterial genome content through distinct mechanisms over different timescales. Nat. Commun. 5:5471 [Google Scholar]
  73. Seed KD, Lazinski DW, Calderwood SB, Camilli A. 73.  2013. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494:489–91 [Google Scholar]
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The Phage-Inducible Chromosomal Islands: A Family of Highly Evolved Molecular Parasites
Annual Review of Virology 2, 181 (2015); https://doi.org/10.1146/annurev-virology-031413-085446
/content/journals/10.1146/annurev-virology-031413-085446
/content/journals/10.1146/annurev-virology-031413-085446
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