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

Annual Review of Virology

Volumn 2, Issue , 2015, Pages 181-201

  Penadés, José R ^a   Christie, Gail E ^b  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Bacteriophage; Evolution; Horizontal gene transfer; Molecular piracy; Pathogenicity island; Virulence

Indexed keywords

TOXIC SHOCK SYNDROME TOXIN 1;

CHROMOSOME MAP; DNA PACKAGING; DNA REPLICATION ORIGIN; ENTEROCOCCUS FAECALIS; GENETIC REGULATION; GENETIC TRANSCRIPTION; GENOME ANALYSIS; HORIZONTAL GENE TRANSFER; MOLECULAR EVOLUTION; MOLECULAR WEIGHT; NONHUMAN; OPEN READING FRAME; OPERON; PATHOGENICITY ISLAND; PHAGE INDUCIBLE CHROMOSOMAL ISLAND; PRIORITY JOURNAL; REVIEW; SOUTHERN BLOTTING; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS SAPROPHYTICUS; VIRUS CAPSID; BACTERIOPHAGE; BACTERIUM; CLASSIFICATION; GENETICS; GENOMIC ISLAND; INTERSPERSED REPEAT; PHYSIOLOGY; VIROLOGY;

BACTERIA; BACTERIOPHAGES; GENOMIC ISLANDS; INTERSPERSED REPETITIVE SEQUENCES;

EID: 84969245534     PISSN: 2327056X     EISSN: 23270578     Source Type: Journal    
DOI: 10.1146/annurev-virology-031413-085446     Document Type: Review

References (73)

1. Freeman VJ. 1951. Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. J. Bacteriol. 61:675-88
2. Wagner PL,Waldor MK. 2002. Bacteriophage control of bacterial virulence. Infect. Immun. 70:3985-93
3. Boyd EF. 2012. Bacteriophage-encoded bacterial virulence factors and phage-pathogenicity island interactions. Adv. Virus Res. 82:91-118
4. BrüssowH,CanchayaC,HardtWD.2004. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol. Mol. Biol. Rev. 68:560-602
5. FortierLC, SekulovicO. 2013. Importance of prophages to evolution and virulence of bacterial pathogens. Virulence 4:354-65
6. Penadés JR, Chen J, Quiles-Puchalt N, Carpena N, Novick RP. 2015. Bacteriophage-mediated spread of bacterial virulence genes. Curr. Opin. Microbiol. 23:171-78
7. Sandri RM, Berger H. 1980. Bacteriophage P1-mediated generalized transduction in Escherichia coli: fate of transduced DNA in rec+ and recA- recipients. Virology 106:14-29
8. Ebel-Tsipis J, Botstein D, Fox MS. 1972. Generalized transduction by phage P22 in Salmonella typhimurium. I. Molecular origin of transducing DNA. J. Mol. Biol. 71:433-48
9. IkedaH,Tomizawa JI. 1965. Transducing fragments in generalized transduction by phageP1. I. Molecular origin of the fragments. J. Mol. Biol. 14:85-109
10. Bergdoll MS, Crass BA, Reiser RF, Robbins RN, Davis JP. 1981. A new staphylococcal enterotoxin, enterotoxin F, associated with toxic-shock-syndrome Staphylococcus aureus isolates. Lancet 1:1017-21
11. Schutzer SE, Fischetti VA, Zabriskie JB. 1983. Toxic shock syndrome and lysogeny in Staphylococcus aureus. Science 220:316-18
12. Kreiswirth BN, Löfdahl S, Betley MJ, O'Reilly M, Schlievert PM, et al. 1983. The toxic shock syndrome exotoxin structural gene is not detectably transmitted by a prophage. Nature 305:709-12
13. Chu MC, Kreiswirth BN, Pattee PA, Novick RP, Melish ME, James JF. 1988. Association of toxic shock toxin-1 determinantwith a heterologous insertion atmultiple loci in the Staphylococcus aureus chromosome. Infect. Immun. 56:2702-8
14. 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. 29:527-43
15. Ruzin A, Lindsay J, Novick RP. 2001. Molecular genetics of SaPI1 - A mobile pathogenicity island in Staphylococcus aureus. Mol. Microbiol. 41:365-77
16. Fitzgerald JR, Monday SR, Foster TJ, Bohach GA, Hartigan PJ, et al. 2001. Characterization of a putative pathogenicity island from bovine Staphylococcus aureus encoding multiple superantigens. J. Bacteriol. 183:63-70
17. Úbeda C, Tormo MA, Cucarella C, Trotonda P, Foster TJ, 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
18. Cucarella C, Solano C, Valle J, Amorena B, Lasa I, Penadés JR. 2001. Bap, a Staphylococcus aureus surface protein involved in biofilm formation. J. Bacteriol. 183:2888-96
19. Úbeda C,Maiques E, Knecht E, Lasa I, Novick RP, Penadés JR. 2005. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol. Microbiol. 56:836-44
20. Novick RP, Christie GE, Penadés JR. 2010. The phage-related chromosomal islands of Gram-positive bacteria. Nat. Rev. Microbiol. 8:541-51
21. Lindqvist BH, Dehò G, Calendar R. 1993. Mechanisms of genome propagation and helper exploitation by satellite phage P4. Microbiol. Rev. 57:683-702
22. Arnold HP, She Q, Phan H, Stedman K, Prangishvili D, 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
23. Maiques E, Úbeda C, Campoy S, Salvador N, Lasa I, et al. 2006. β-Lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J. Bacteriol. 188:2726-29
24. Selva L, Viana D, Regev-Yochay G, Trzcinski K, Corpa JM, et al. 2009. Killing niche competitors by remote-control bacteriophage induction. PNAS 106:1234-38
25. Chen J, Novick RP. 2009. Phage-mediated intergeneric transfer of toxin genes. Science 323:139-41
26. Maiques E, Úbeda C, TormoMA, FerrerMD, Lasa I, et al. 2007. Role of staphylococcal phage and SaPI integrase in intra-and interspecies SaPI transfer. J. Bacteriol. 189:5608-16
27. Chen J, Carpena N, Quiles-Puchalt N, Ram G, Novick RP, Penadés JR. 2014. Intra-and inter-generic transfer of pathogenicity island-encoded virulence genes by cos phages. ISME J. 9:1260-63
28. Winstel V, Liang C, Sanchez-Carballo P, Steglich M, Munar M, et al. 2013. Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens. Nat. Commun. 4:2345
29. Tormo-Más MA, Mir I, Shrestha A, Tallent SM, Campoy S, et al. 2010. Moonlighting bacteriophage proteins derepress staphylococcal pathogenicity islands. Nature 465:779-82
30. Úbeda C,Maiques E, Barry P,Matthews A, TormoMA, et al. 2008. SaPI mutations affecting replication and transfer and enabling autonomous replication in the absence of helper phage. Mol. Microbiol. 67:493-503
31. Lane KD.2013. Transcriptional crosstalk between helper bacteriophages and Staphylococcus aureus pathogenicity islands. PhD Diss., Va. Commonw. Univ., Richmond
32. Campbell A. 2007. Phage integration and chromosome structure. A personal history. Annu. Rev. Genet. 41:1-11
33. Subedi A, Úbeda C, Adhikari RP, Penadés JR, Novick RP. 2007. Sequence analysis reveals genetic exchanges and intraspecific spread of SaPI2, a pathogenicity island involved in menstrual toxic shock. Microbiology 153:3235-45
34. Mir-Sanchis I, Martínez-Rubio R, Martí M, Chen J, Lasa I, et al. 2012. Control of Staphylococcus aureus pathogenicity island excision. Mol. Microbiol. 85:833-45
35. Úbeda C, Barry P, Penadés JR, Novick RP. 2007. A pathogenicity island replicon in Staphylococcus aureus replicates as an unstable plasmid. PNAS 104:14182-88
36. Úbeda C, Tormo-Más MA, Penadés JR, Novick RP. 2012. Structure-function analysis of the SaPIbov1 replication origin in Staphylococcus aureus. Plasmid 67:183-90
37. Úbeda C, Maiques E, Tormo MA, Campoy S, Lasa I, et al. 2007. SaPI operon I is required for SaPI packaging and is controlled by LexA. Mol. Microbiol. 65:41-50
38. 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
39. Chen J, Ram G, Penadés JR, Brown S, Novick RP. 2015. Pathogenicity island-directed transfer of unlinked chromosomal virulence genes. Mol. Cell 57:138-49
40. Ram G, Chen J, Kumar K, Ross HF, Úbeda C, et al. 2012. Staphylococcal pathogenicity island interference with helper phage reproduction is a paradigm of molecular parasitism. PNAS 109:16300-5
41. Poliakov A, Chang JR, Spilman MS, Damle PK, Christie GE, 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
42. Úbeda C, Olivarez NP, Barry P, Wang H, Kong X, et al. 2009. Specificity of staphylococcal phage and SaPI DNA packaging as revealed by integrase and terminase mutations. Mol. Microbiol. 72:98-108
43. RamG, Chen J, Ross HF,Novick RP. 2014. Preciselymodulated pathogenicity island interference with late phage gene transcription. PNAS 111:14536-41
44. Harwich MD. 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. 2010. Mobile genetic elements of Staphylococcus aureus. Cell. Mol. Life Sci. 67:3057-71
46. VianaD, Blanco J, Tormo-MásMA, Selva L,Guinane CM, 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
47. Guinane CM, Ben Zakour NL, Tormo-Más MA, Weinert LA, Lowder BV, 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
48. O'Neill AJ, Larsen AR, SkovR,Henriksen AS,Chopra I. 2007. Characterization of the epidemic European fusidic acid-resistant impetigo clone of Staphylococcus aureus. J. Clin. Microbiol. 45:1505-10
49. Chen HJ, Chang YC, Tsai JC, Hung WC, Lin YT, 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
50. Kuroda M, Yamashita A, Hirakawa H, Kumano M, Morikawa K, et al. 2005. Whole genome sequence of Staphylococcus saprophyticus reveals the pathogenesis of uncomplicated urinary tract infection. PNAS 102:13272-77
51. Christie GE, Dokland T. 2012. Pirates of the Caudovirales. Virology 434:210-21
52. Damle PK, Wall EA, Spilman MS, Dearborn AD, Ram G, et al. 2012. The roles of SaPI1 proteins gp7 (CpmA) and gp6 (CpmB) in capsid size determination and helper phage interference. Virology 432:277-82
53. Tormo-Más MA, Donderis J, García-Caballer M, Alt A, Mir-Sanchis I, et al. 2013. Phage dUTPases control transfer of virulence genes by a proto-oncogenic G protein-like mechanism. Mol. Cell 49:947-58
54. Tallent SM, Christie GE. 2007. Transducing particles of Staphylococcus aureus pathogenicity island SaPI1 are comprised of helper phage-encoded proteins. J. Bacteriol. 189:7520-24
55. Tormo MA, Ferrer MD, Maiques E, Úbeda C, Selva L, et al. 2008. Staphylococcus aureus pathogenicity island DNA is packaged in particles composed of phage proteins. J. Bacteriol. 190:2434-40
56. Quiles-Puchalt N, Carpena N, Alonso JC, Novick RP, Marina A, Penadés JR. 2014. Staphylococcal pathogenicity island DNA packaging system involving cos-site packaging and phage-encoded HNH endonucleases. PNAS 111:6016-21
57. Dearborn AD, Dokland T. 2012. Mobilization of pathogenicity islands by Staphylococcus aureus strain Newman bacteriophages. Bacteriophage 2:70-78
58. Liu J, Dehbi M, Moeck G, Arhin F, Bauda P, et al. 2004. Antimicrobial drug discovery through bacteriophage genomics. Nat. Biotechnol. 22:185-91
59. Spilman MS, Dearborn AD, Chang JR, Damle PK, Christie GE, Dokland T. 2011. A conformational switch involved in maturation of Staphylococcus aureus bacteriophage 80αcapsids. J. Mol. Biol. 405:863-76
60. Quiles-Puchalt N, Martínez-Rubio R, Ram G, Lasa I, Penadés JR. 2014. Unravelling bacteriophagePdbl11 requirements for packaging and transfer of mobile genetic elements in Staphylococcus aureus. Mol. Microbiol. 91:423-37
61. Dearborn AD, Spilman MS, Damle PK, Chang JR, Monroe EB, 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
62. Spilman MS,Damle PK,Dearborn AD, RodenburgCM, Chang JR, et al. 2012. Assembly of bacteriophage 80αcapsids in a Staphylococcus aureus expression system. Virology 434:242-50
63. Christie GE, Matthews AM, King DG, Lane KD, Olivarez NP, et al. 2010. The complete genomes of Staphylococcus aureus bacteriophages 80 and 80α-implications for the specificity of SaPI mobilization. Virology 407:381-90
64. Feiss M, Rao VB. 2012. The bacteriophage DNA packaging machine. Adv. Exp. Med. Biol. 726:489-509
65. Quiles-PuchaltN,Tormo-MásMA,Campoy S,Toledo-Arana A,MonederoV, et al. 2013. A super-family of transcriptional activators regulates bacteriophage packaging and lysis inGram-positive bacteria. Nucleic Acids Res. 41:7260-75
66. Ferrer MD, Quiles-Puchalt N, Harwich MD, Tormo-Más MA, Campoy S, et al. 2011. RinA controls phage-mediated packaging and transfer of virulence genes in Gram-positive bacteria. Nucleic Acids Res. 39:5866-78
67. Duerkop BA, Clements CV, Rollins D, Rodrigues JLM, Hooper LV. 2012. A composite bacteriophage alters colonization by an intestinal commensal bacterium. PNAS 109:17621-26
68. Matos RC, Lapaque N, Rigottier-Gois L, Debarbieux L, Meylheuc T, et al. 2013. Enterococcus faecalis prophage dynamics and contributions to pathogenic traits. PLOS Genet. 9:e1003539
69. Scott J, Thompson-Mayberry P, Lahmamsi S, King CJ, McShan WM. 2008. Phage-associated mutator phenotype in group A streptococcus. J. Bacteriol. 190:6290-301
70. Scott J, Nguyen SV, King CJ, Hendrickson C, McShan WM. 2012. Phage-like Streptococcus pyogenes chromosomal islands (SpyCI) and mutator phenotypes: control by growth state and rescue by a SpyCIencoded promoter. Front. Microbiol. 3:317
71. Nguyen SV, McShanWM. 2014. Chromosomal islands of Streptococcus pyogenes and related streptococci: molecular switches for survival and virulence. Front. Cell. Infect. Microbiol. 4:109
72. Croucher NJ, Coupland PG, Stevenson AE, Callendrello A, Bentley SD, Hanage WP. 2014. Diversification of bacterial genome content through distinct mechanisms over different timescales. Nat. Commun. 5:5471
73. Seed KD, LazinskiDW, Calderwood SB, Camilli A. 2013. A bacteriophage encodes its own CRISPR/Cas adaptive response to evade host innate immunity. Nature 494:489-91