Enterococcus faecalis Prophage Dynamics and Contributions to Pathogenic Traits

PLoS Genetics

Volumn 9, Issue 6, 2013, Pages

  Matos, Renata C ^a,b   Lapaque, Nicolas ^a   Rigottier Gois, Lionel ^a   Debarbieux, Laurent ^c   Meylheuc, Thierry ^a   Gonzalez Zorn, Bruno ^d   Repoila, Francis ^a   de Lopes, Maria Fatima ^b,e   Serror, Pascale ^a  

^a UMR1319 MICALIS   (France)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^c INSTITUT PASTEUR   (France)

^d UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^e IBET   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; PLATELET BINDING PROTEIN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL CHROMOSOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BIOLOGICAL TRAIT; CONTROLLED STUDY; ENTEROCOCCUS FAECALIS; GENE INTERACTION; GRAM POSITIVE BACTERIUM; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PROPHAGE; PROTEIN FUNCTION; STAPHYLOCOCCUS; THROMBOCYTE ADHESION; VIRION; VIROGENESIS; VIRUS CAPSID;

CHROMOSOMES, BACTERIAL; CROSS INFECTION; ENTEROCOCCUS FAECALIS; GENOME, BACTERIAL; HOST-PATHOGEN INTERACTIONS; HUMANS; PROPHAGES; VIRULENCE FACTORS; VIRUS ACTIVATION;

BACTERIA (MICROORGANISMS); ENTEROCOCCUS FAECALIS; MIRIDAE; POSIBACTERIA; STAPHYLOCOCCUS;

EID: 84879663855     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003539     Document Type: Article

References (91)

1. Wagner PL, Waldor MK, (2002) Bacteriophage control of bacterial virulence. Infect Immun 70: 3985-3993.
2. Thomas CM, Nielsen KM, (2005) Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol 3: 711-721.
3. Chen J, Novick RP, (2009) Phage-mediated intergeneric transfer of toxin genes. Science 323: 139-141.
4. Freeman VJ, (1951) Studies on the virulence of bacteriophage-infected strains of Corynebacterium diphtheriae. J Bacteriol 61: 675-688.
5. O'Brien AD, Newland JW, Miller SF, Holmes RK, Smith HW, et al. (1984) Shiga-like toxin-converting phages from Escherichia coli strains that cause hemorrhagic colitis or infantile diarrhea. Science 226: 694-696.
6. Davis BM, Waldor MK, (2003) Filamentous phages linked to virulence of Vibrio cholerae. Curr Opin Microbiol 6: 35-42.
7. Brussow H, Canchaya C, Hardt W-D, (2004) Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68: 560-602.
8. Desiere F, Lucchini S, Canchaya C, Ventura M, Brussow H, (2002) Comparative genomics of phages and prophages in lactic acid bacteria. Antonie Van Leeuwenhoek 82: 73-91.
9. Casjens S, (2003) Prophages and bacterial genomics: what have we learned so far? Mol Microbiol 49: 277-300.
10. Sun J, Barbieri JT, (2003) Pseudomonas aeruginosa ExoT ADP-ribosylates CT10 regulator of kinase (Crk) proteins. J Biol Chem 278: 32794-32800.
11. Chinnapen DJ, Chinnapen H, Saslowsky D, Lencer WI, (2007) Rafting with cholera toxin: endocytosis and trafficking from plasma membrane to ER. FEMS Microbiol Lett 266: 129-137.
12. Kim YH, Lee Y, Kim S, Yeom J, Yeom S, et al. (2006) The role of periplasmic antioxidant enzymes (superoxide dismutase and thiol peroxidase) of the Shiga toxin-producing Escherichia coli O157:H7 in the formation of biofilms. Proteomics 6: 6181-6193.
13. Mirold S, Rabsch W, Rohde M, Stender S, Tschape H, et al. (1999) Isolation of a temperate bacteriophage encoding the type III effector protein SopE from an epidemic Salmonella typhimurium strain. Proc Natl Acad Sci U S A 96: 9845-9850.
14. Figueroa-Bossi N, Bossi L, (1999) Inducible prophages contribute to Salmonella virulence in mice. Mol Microbiol 33: 167-176.
15. Figueroa-Bossi N, Uzzau S, Maloriol D, Bossi L, (2001) Variable assortment of prophages provides a transferable repertoire of pathogenic determinants in Salmonella. Mol Microbiol 39: 260-271.
16. Coleman D, Knights J, Russell R, Shanley D, Birkbeck TH, et al. (1991) Insertional inactivation of the Staphylococcus aureus beta-toxin by bacteriophage phi 13 occurs by site- and orientation-specific integration of the phi 13 genome. Mol Microbiol 5: 933-939.
17. Rabinovich L, Sigal N, Borovok I, Nir-Paz R, Herskovits AA, (2012) Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence. Cell 150: 792-802.
18. Wagner PL, Livny J, Neely MN, Acheson DW, Friedman DI, et al. (2002) Bacteriophage control of Shiga toxin 1 production and release by Escherichia coli. Mol Microbiol 44: 957-970.
19. Bensing BA, Siboo IR, Sullam PM, (2001) Proteins PblA and PblB of Streptococcus mitis, which promote binding to human platelets, are encoded within a lysogenic bacteriophage. Infect Immun 69: 6186-6192.
20. Subedi A, Ubeda C, Adhikari RP, Penades JR, Novick RP, (2007) Sequence analysis reveals genetic exchanges and intraspecific spread of SaPI2, a pathogenicity island involved in menstrual toxic shock. Microbiology 153: 3235-3245.
21. Mizutani S, Nakazono N, Sugino Y, (1999) The so-called chromosomal verotoxin genes are actually carried by defective prophages. DNA Res 6: 141-143.
22. Dahan S, Wiles S, La Ragione RM, Best A, Woodward MJ, et al. (2005) EspJ is a prophage-carried type III effector protein of attaching and effacing pathogens that modulates infection dynamics. Infect Immun 73: 679-686.
23. 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.
24. 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 SpyCI-Encoded Promoter. Front Microbiol 3: 317.
25. Tallent SM, Langston TB, Moran RG, Christie GE, (2007) Transducing particles of Staphylococcus aureus pathogenicity island SaPI1 are comprised of helper phage-encoded proteins. J Bacteriol 189: 7520-7524.
26. Novick RP, Christie GE, Penades JR, (2010) The phage-related chromosomal islands of Gram-positive bacteria. Nat Rev Microbiol 8: 541-551.
27. Christie GE, Dokland T, (2012) Pirates of the Caudovirales. Virology 434: 210-221.
28. Ubeda C, Maiques E, Barry P, Matthews A, Tormo MA, et al. (2008) SaPI mutations affecting replication and transfer and enabling autonomous replication in the absence of helper phage. Mol Microbiol 67: 493-503.
29. Ruzin A, Lindsay J, Novick RP, (2001) Molecular genetics of SaPI1-a mobile pathogenicity island in Staphylococcus aureus. Mol Microbiol 41: 365-377.
30. Maiques E, Ubeda C, Tormo MA, Ferrer MD, Lasa I, et al. (2007) Role of staphylococcal phage and SaPI integrase in intra- and interspecies SaPI transfer. J Bacteriol 189: 5608-5616.
31. Ram G, Chen J, Kumar K, Ross HF, Ubeda C, et al. (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.
32. 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.
33. Wang X, Kim Y, Ma Q, Hong SH, Pokusaeva K, et al. (2010) Cryptic prophages help bacteria cope with adverse environments. Nat Commun 1: 147.
34. Tree JJ, Roe AJ, Flockhart A, McAteer SP, Xu X, et al. (2011) Transcriptional regulators of the GAD acid stress island are carried by effector protein-encoding prophages and indirectly control type III secretion in enterohemorrhagic Escherichia coli O157:H7. Mol Microbiol 80: 1349-1365.
35. Bae T, Baba T, Hiramatsu K, Schneewind O, (2006) Prophages of Staphylococcus aureus Newman and their contribution to virulence. Mol Microbiol 62: 1035-1047.
36. Bossi L, Fuentes JA, Mora G, Figueroa-Bossi N, (2003) Prophage contribution to bacterial population dynamics. J Bacteriol 185: 6467-6471.
37. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, et al. (2010) A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464: 59-65.
38. Arias CA, Murray BE, (2012) The rise of the Enterococcus: beyond vancomycin resistance. Nat Rev Microbiol 10: 266-278.
39. Freitas AR, Novais C, Ruiz-Garbajosa P, Coque TM, Peixe L, (2009) Dispersion of multidrug-resistant Enterococcus faecium isolates belonging to major clonal complexes in different Portuguese settings. Appl Environ Microbiol 75: 4904-4908.
40. Kuch A, Willems RJ, Werner G, Coque TM, Hammerum AM, et al. (2012) Insight into antimicrobial susceptibility and population structure of contemporary human Enterococcus faecalis isolates from Europe. J Antimicrob Chemother 67: 551-558.
41. Nallapareddy SR, Wenxiang H, Weinstock GM, Murray BE, (2005) Molecular characterization of a widespread, pathogenic, and antibiotic resistance-receptive Enterococcus faecalis lineage and dissemination of its putative pathogenicity island. J Bacteriol 187: 5709-5718.
42. Sahm DF, Kissinger J, Gilmore MS, Murray PR, Mulder R, et al. (1989) In vitro susceptibility studies of vancomycin-resistant Enterococcus faecalis. Antimicrob Agents Chemother 33: 1588-1591.
43. Paulsen IT, Banerjei L, Myers GS, Nelson KE, Seshadri R, et al. (2003) Role of mobile DNA in the evolution of vancomycin-resistant Enterococcus faecalis. Science 299: 2071-2074.
44. McBride SM, Fischetti VA, Leblanc DJ, Moellering RC Jr, Gilmore MS, (2007) Genetic diversity among Enterococcus faecalis. PLoS ONE 2: e582.
45. Solheim M, Brekke MC, Snipen LG, Willems RJ, Nes IF, et al. (2011) Comparative genomic analysis reveals significant enrichment of mobile genetic elements and genes encoding surface structure-proteins in hospital-associated clonal complex 2 Enterococcus faecalis. BMC Microbiol 11: 3.
46. Yasmin A, Kenny JG, Shankar J, Darby AC, Hall N, et al. (2010) Comparative genomics and transduction potential of Enterococcus faecalis temperate bacteriophages. J Bacteriol 192: 1122-1130.
47. Fieldhouse RJ, Turgeon Z, White D, Merrill AR, (2010) Cholera- and anthrax-like toxins are among several new ADP-ribosyltransferases. PLoS Comput Biol 6: e1001029.
48. Botstein D, (1980) A theory of modular evolution for bacteriophages. Ann N Y Acad Sci 354: 484-490.
49. Campbell A, (1994) Comparative molecular biology of lambdoid phages. Annu Rev Microbiol 48: 193-222.
50. Hirano N, Muroi T, Takahashi H, Haruki M, (2011) Site-specific recombinases as tools for heterologous gene integration. Appl Microbiol Biotechnol 92: 227-239.
51. Lepage E, Brinster S, Caron C, Ducroix-Crepy C, Rigottier-Gois L, et al. (2006) Comparative genomic hybridization analysis of Enterococcus faecalis: identification of genes absent from food strains. J Bacteriol 188: 6858-6868.
52. Waldor MK, Friedman DI, (2005) Phage regulatory circuits and virulence gene expression. Curr Opin Microbiol 8: 459-465.
53. Rigottier-Gois L, Alberti A, Houel A, Taly JF, Palcy P, et al. (2011) Large-Scale Screening of a Targeted Enterococcus faecalis Mutant Library Identifies Envelope Fitness Factors. PLoS One 6: e29023.
54. Bourgogne A, Garsin DA, Qin X, Singh KV, Sillanpaa J, et al. (2008) Large scale variation in Enterococcus faecalis illustrated by the genome analysis of strain OG1RF. Genome Biol 9: R110.
55. Lemire S, Figueroa-Bossi N, Bossi L, (2011) Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors. PLoS Genet 7: e1002149.
56. Palmer KL, Godfrey P, Griggs A, Kos VN, Zucker J, et al. (2012) Comparative genomics of enterococci: variation in Enterococcus faecalis, clade structure in E. faecium, and defining characteristics of E. gallinarum and E. casseliflavus. MBio 3: e00318-00311.
57. Kropinski AM, Prangishvili D, Lavigne R, (2009) Position paper: The creation of a rational scheme for the nomenclature of viruses of Bacteria and Archaea. Environmental Microbiology 11: 2775-2777.
58. Duerkop BA, Clements CV, Rollins D, Rodrigues JL, Hooper LV, (2012) A composite bacteriophage alters colonization by an intestinal commensal bacterium. Proc Natl Acad Sci U S A 109: 17621-17626.
59. Marrero R, Lovett PS, (1982) Interference of plasmid pCM194 with lysogeny of bacteriophage SP02 in Bacillus subtilis. J Bacteriol 152: 284-290.
60. Reynolds RB, Reddy A, Thorne CB, (1988) Five unique temperate phages from a polylysogenic strain of Bacillus thuringiensis subsp. aizawai. J Gen Microbiol 134: 1577-1585.
61. Espeland EM, Lipp EK, Huq A, Colwell RR, (2004) Polylysogeny and prophage induction by secondary infection in Vibrio cholerae. Environ Microbiol 6: 760-763.
62. Asadulghani M, Ogura Y, Ooka T, Itoh T, Sawaguchi A, et al. (2009) The defective prophage pool of Escherichia coli O157: prophage-prophage interactions potentiate horizontal transfer of virulence determinants. PLoS Pathog 5: e1000408.
63. Figueroa-Bossi N, Coissac E, Netter P, Bossi L, (1997) Unsuspected prophage-like elements in Salmonella typhimurium. Mol Microbiol 25: 161-173.
64. Boyd EF, Brussow H, (2002) Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol 10: 521-529.
65. Friedman DI, Mozola CC, Beeri K, Ko CC, Reynolds JL, (2011) Activation of a prophage-encoded tyrosine kinase by a heterologous infecting phage results in a self-inflicted abortive infection. Mol Microbiol 82: 567-577.
66. Ubeda 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.
67. Tormo-Mas MA, Donderis J, Garcia-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.
68. Tormo-Mas MA, Mir I, Shrestha A, Tallent SM, Campoy S, et al. (2010) Moonlighting bacteriophage proteins derepress staphylococcal pathogenicity islands. Nature 465: 779-782.
69. Scott J, Thompson-Mayberry P, Lahmamsi S, King CJ, McShan WM, (2008) Phage-associated mutator phenotype in group A streptococcus. J Bacteriol 190: 6290-6301.
70. Ubeda 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.
71. Dearborn AD, Dokland T, (2012) Mobilization of pathogenicity islands by Staphylococcus aureus strain Newman bacteriophages. Bacteriophage 2: 70-78.
72. Oppenheim AB, Kobiler O, Stavans J, Court DL, Adhya S, (2005) Switches in bacteriophage lambda development. Annu Rev Genet 39: 409-429.
73. Dwyer DJ, Kohanski MA, Collins JJ, (2009) Role of reactive oxygen species in antibiotic action and resistance. Curr Opin Microbiol 12: 482-489.
74. Mitchell J, Siboo IR, Takamatsu D, Chambers HF, Sullam PM, (2007) Mechanism of cell surface expression of the Streptococcus mitis platelet binding proteins PblA and PblB. Mol Microbiol 64: 844-857.
75. Campoy S, Hervas A, Busquets N, Erill I, Teixido L, et al. (2006) Induction of the SOS response by bacteriophage lytic development in Salmonella enterica. Virology 351: 360-367.
76. Canchaya C, Fournous G, Chibani-Chennoufi S, Dillmann ML, Brussow H, (2003) Phage as agents of lateral gene transfer. Curr Opin Microbiol 6: 417-424.
77. Mazaheri Nezhad Fard R, Barton MD, Heuzenroeder MW, (2011) Bacteriophage-mediated transduction of antibiotic resistance in enterococci. Lett Appl Microbiol 52: 559-564.
78. Hastings PJ, Rosenberg SM, Slack A, (2004) Antibiotic-induced lateral transfer of antibiotic resistance. Trends Microbiol 12: 401-404.
79. Goerke C, Koller J, Wolz C, (2006) Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob Agents Chemother 50: 171-177.
80. Zhang X, McDaniel AD, Wolf LE, Keusch GT, Waldor MK, et al. (2000) Quinolone antibiotics induce Shiga toxin-encoding bacteriophages, toxin production, and death in mice. J Infect Dis 181: 664-670.
81. Ubeda C, Maiques E, Knecht E, Lasa I, Novick RP, et al. (2005) Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in staphylococci. Mol Microbiol 56: 836-844.
82. Selva L, Viana D, Regev-Yochay G, Trzcinski K, Corpa JM, et al. (2009) Killing niche competitors by remote-control bacteriophage induction. Proc Natl Acad Sci U S A 106: 1234-1238.
83. Carmeli Y, Eliopoulos GM, Samore MH, (2002) Antecedent treatment with different antibiotic agents as a risk factor for vancomycin-resistant Enterococcus. Emerg Infect Dis 8: 802-807.
84. Brown SP, Le Chat L, De Paepe M, Taddei F, (2006) Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare. Curr Biol 16: 2048-2052.
85. Godeke J, Paul K, Lassak J, Thormann KM, (2011) Phage-induced lysis enhances biofilm formation in Shewanella oneidensis MR-1. Isme J 5: 613-626.
86. Rice SA, Tan CH, Mikkelsen PJ, Kung V, Woo J, et al. (2009) The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. Isme J 3: 271-282.
87. Carrolo M, Frias MJ, Pinto FR, Melo-Cristino J, Ramirez M, (2010) Prophage spontaneous activation promotes DNA release enhancing biofilm formation in Streptococcus pneumoniae. PLoS One 5: e15678.
88. Brinster S, Furlan S, Serror P, (2007) C-terminal WxL domain mediates cell wall binding in Enterococcus faecalis and other gram-positive bacteria. J Bacteriol 189: 1244-1253.
89. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor. Cold Spring Harbor Laboratory Press.
90. Pultz NJ, Shankar N, Baghdayan AS, Donskey CJ, (2005) Enterococcal surface protein Esp does not facilitate intestinal colonization or translocation of Enterococcus faecalis in clindamycin-treated mice. FEMS Microbiology Letters 242: 217-219.
91. Maddox SM, Coburn PS, Shankar N, Conway T, (2012) Transcriptional regulator PerA influences biofilm-associated, platelet binding, and metabolic gene expression in Enterococcus faecalis. PLoS One 7: e34398.