A novel Pseudomonas aeruginosa bacteriophage, Ab31, a chimera formed from temperate phage PAJU2 and P. putida lytic phage AF: Characteristics and mechanism of bacterial resistance

PLoS ONE

Volumn 9, Issue 4, 2014, Pages

  Latino, Libera ^a,b   Essoh, Christiane ^a,b   Blouin, Yann ^a,b   Vu Thien, Hoang ^c   Pourcel, Christine ^a,b  

^a INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^b CNRS   (France)

^c ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINIC ACID;

AB31 GENE; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COLONIZATION; BACTERIAL GENOME; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIOPHAGE; BACTERIOPHAGE AF; BACTERIOPHAGE PAJU2; BACTERIUM ISOLATE; CHIMERA; CONTROLLED STUDY; CYSTIC FIBROSIS; GENE; GENE CLUSTER; GENE DELETION; GENE FUNCTION; GENE IDENTIFICATION; GENE INSERTION; GENE SEQUENCE; GENETIC VARIABILITY; GENOME ANALYSIS; HOST PATHOGEN INTERACTION; LUNG INFECTION; NEW SPECIES; NONHUMAN; PHENOTYPE; PSEUDOMONAS PHAGE; SPECIES COMPARISON; SPECIES DIFFERENCE; GENETICS; HUMAN; MICROBIOLOGY; PSEUDOMONAS AERUGINOSA;

CHIMERA; CYSTIC FIBROSIS; DRUG RESISTANCE, BACTERIAL; HUMANS; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS PHAGES;

EID: 84899426269     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0093777     Document Type: Article

References (58)

1. Penketh AR, Wise A, Mearns MB, Hodson ME, Batten JC (1987) Cystic fibrosis in adolescents and adults. Thorax 42: 526-532. (Pubitemid 17097058)
2. Brussow H (2012) Pseudomonas biofilms, cystic fibrosis, and phage: a silver lining? MBio 3.
3. Hogardt M, Heesemann J (2010) Adaptation of Pseudomonas aeruginosa during persistence in the cystic fibrosis lung. Int J Med Microbiol 300: 557-562.
4. Flemming HC, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8: 623-633.
5. Schurks N, Wingender J, Flemming HC, Mayer C (2002) Monomer composition and sequence of alginates from Pseudomonas aeruginosa. Int J Biol Macromol 30: 105-111. (Pubitemid 34242689)
6. Qiu D, Eisinger VM, Rowen DW, Yu HD (2007) Regulated proteolysis controls mucoid conversion in Pseudomonas aeruginosa . Proc Natl Acad Sci U S A 104: 8107-8112. (Pubitemid 47185883)
7. Al-Dujaili AH, Harris DM (1975) Pseudomonas aeruginosa infection in hospital: a comparison between 'infective' and 'environmental' strains. J Hyg (Lond) 75: 195-201.
8. Miller RV, Rubero VJ (1984) Mucoid conversion by phages of Pseudomonas aeruginosa strains from patients with cystic fibrosis. J Clin Microbiol 19: 717-719. (Pubitemid 14142671)
9. Hosseinidoust Z, Tufenkji N, van de Ven TG (2013) Predation in homogeneous and heterogeneous phage environments affects virulence determinants of Pseudomonas aeruginosa . Appl Environ Microbiol 79: 2862-2871.
10. Hosseinidoust Z, van de Ven TG, Tufenkji N (2013) Evolution of Pseudomonas aeruginosa virulence as a result of phage predation. Appl Environ Microbiol 79: 6110-6116.
11. Ceyssens PJ, Lavigne R (2010) Bacteriophages of Pseudomonas. Future Microbiol 5: 1041-1055.
12. Hatfull GF (2008) Bacteriophage genomics. Curr Opin Microbiol 11: 447-453.
13. Hatfull GF, Hendrix RW (2011) Bacteriophages and their genomes. Curr Opin Virol 1: 298-303.
14. Essoh C, Blouin Y, Loukou G, Cablanmian A, Lathro S, et al. (2013) The Susceptibility of Pseudomonas aeruginosa Strains from Cystic Fibrosis Patients to Bacteriophages. PLoS One 8: e60575.
15. Lu S, Le S, Tan Y, Zhu J, Li M, et al. (2013) Genomic and proteomic analyses of the terminally redundant genome of the Pseudomonas aeruginosa phage PaP1: establishment of genus PaP1-like phages. PLoS One 8: e62933.
16. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG, et al. (1995) Common virulence factors for bacterial pathogenicity in plants and animals. Science 268: 1899-1902.
17. Holloway BW (1955) Genetic recombination in Pseudomonas aeruginosa. J Gen Microbiol 13: 572-581.
18. Romling U, Wingender J, Muller H, Tummler B (1994) A major Pseudomonas aeruginosa clone common to patients and aquatic habitats. Appl Environ Microbiol 60: 1734-1738. (Pubitemid 24165812)
19. Vu-Thien H, Corbineau G, Hormigos K, Fauroux B, Corvol H, et al. (2007) Multiple-locus variable-number tandem-repeat analysis for longitudinal survey of sources of Pseudomonas aeruginosa infection in cystic fibrosis patients. J Clin Microbiol 45: 3175-3183. (Pubitemid 47585637)
20. Llanes C, Pourcel C, Richardot C, Plesiat P, Fichant G, et al. (2013) Diversity of beta-lactam resistance mechanisms in cystic fibrosis isolates of Pseudomonas aeruginosa : a French multicentre study. J Antimicrob Chemother 68: 1763-1771.
21. Brokopp CD, Gomez-Lus R, Farmer JJ, 3rd (1977) Serological typing of Pseudomonas aeruginosa: use of commercial antisera and live antigens. J Clin Microbiol 5: 640-649. (Pubitemid 8137878)
22. Cameron JR, Philippsen P, Davis RW (1977) Analysis of chromosomal integration and deletions of yeast plasmids. Nucleic Acids Res 4: 1429-1448. (Pubitemid 8102397)
23. Van Domselaar GH, Stothard P, Shrivastava S, Cruz JA, Guo A, et al. (2005) BASys: a web server for automated bacterial genome annotation. Nucleic Acids Res 33: W455-459. (Pubitemid 44529961)
24. Cramer N, Klockgether J, Wrasman K, Schmidt M, Davenport CF, et al. (2011) Microevolution of the major common Pseudomonas aeruginosa clones C and PA14 in cystic fibrosis lungs. Environ Microbiol 13: 1690-1704.
25. Xu J, Zhang J, Lu X, Liang W, Zhang L, et al. (2013) O antigen is the receptor of Vibrio cholerae serogroup O1 El Tor typing phage VP4. J Bacteriol 195: 798-806.
26. Cornelissen A, Ceyssens PJ, Krylov VN, Noben JP, Volckaert G, et al. (2012) Identification of EPS-degrading activity within the tail spikes of the novel Pseudomonas putida phage AF. Virology.
27. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S (2004) Bacterial persistence as a phenotypic switch. Science 305: 1622-1625. (Pubitemid 39296357)
28. Crosa JH (1989) Genetics and molecular biology of siderophore-mediated iron transport in bacteria. Microbiol Rev 53: 517-530.
29. Kwan T, Liu J, Dubow M, Gros P, Pelletier J (2006) Comparative genomic analysis of 18 Pseudomonas aeruginosa bacteriophages. J Bacteriol 188: 1184-1187. (Pubitemid 43146437)
30. Wei H, Therrien C, Blanchard A, Guan S, Zhu Z (2008) The Fidelity Index provides a systematic quantitation of star activity of DNA restriction endonucleases. Nucleic Acids Res 36: e50.
31. Uchiyama J, Rashel M, Takemura I, Kato S, Ujihara T, et al. (2012) Genetic characterization of Pseudomonas aeruginosa bacteriophage KPP10. Arch Virol 157: 733-738.
32. Perry LL, SanMiguel P, Minocha U, Terekhov AI, Shroyer ML, et al. (2009) Sequence analysis of Escherichia coli O157:H7 bacteriophage PhiV10 and identification of a phage-encoded immunity protein that modifies the O157 antigen. FEMS Microbiol Lett 292: 182-186.
33. Kropinski AM, Kovalyova IV, Billington SJ, Patrick AN, Butts BD, et al. (2007) The genome of epsilon15, a serotype-converting, Group E1 Salmonella enterica-specific bacteriophage. Virology 369: 234-244. (Pubitemid 350087186)
34. Roos WH, Ivanovska IL, Evilevitch A, Wuite GJ (2007) Viral capsids: mechanical characteristics, genome packaging and delivery mechanisms. Cell Mol Life Sci 64: 1484-1497. (Pubitemid 46954149)
35. Lee DG, Urbach JM, Wu G, Liberati NT, Feinbaum RL, et al. (2006) Genomic analysis reveals that Pseudomonas aeruginosa virulence is combinatorial. Genome Biol 7: R90.
36. Ruer S, Stender S, Filloux A, de Bentzmann S (2007) Assembly of fimbrial structures in Pseudomonas aeruginosa: functionality and specificity of chaperoneusher machineries. J Bacteriol 189: 3547-3555. (Pubitemid 46668819)
37. Jiang X, Jiang H, Li C, Wang S, Mi Z, et al. (2011) Sequence characteristics of T4-like bacteriophage IME08 benome termini revealed by high throughput sequencing. Virol J 8: 194.
38. 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. (Pubitemid 33639753)
39. Steven AC, Trus BL, Maizel JV, Unser M, Parry DA, et al. (1988) Molecular substructure of a viral receptor-recognition protein. The gp17 tail-fiber of bacteriophage T7. J Mol Biol 200: 351-365.
40. Cornelissen A, Ceyssens PJ, T'Syen J, Van Praet H, Noben JP, et al. (2011) The T7-related Pseudomonas putida phage phi15 displays virion-associated biofilm degradation properties. PLoS One 6: e18597.
41. Casjens SR, Molineux IJ (2012) Short noncontractile tail machines: adsorption and DNA delivery by podoviruses. Adv Exp Med Biol 726: 143-179.
42. Friman VP, Ghoul M, Molin S, Johansen HK, Buckling A (2013) Pseudomonas aeruginosa Adaptation to Lungs of Cystic Fibrosis Patients Leads to Lowered Resistance to Phage and Protist Enemies. PLoS One 8: e75380.
43. Uchiyama J, Rashel M, Matsumoto T, Sumiyama Y, Wakiguchi H, et al. (2009) Characteristics of a novel Pseudomonas aeruginosa bacteriophage, PAJU2, which is genetically related to bacteriophage D3. Virus Res 139: 131-134.
44. Mooij MJ, Drenkard E, Llamas MA, Vandenbroucke-Grauls CM, Savelkoul PH, et al. (2007) Characterization of the integrated filamentous phage Pf5 and its involvement in small-colony formation. Microbiology 153: 1790-1798. (Pubitemid 46952509)
45. Webb JS, Lau M, Kjelleberg S (2004) Bacteriophage and phenotypic variation in Pseudomonas aeruginosa biofilm development. J Bacteriol 186: 8066-8073. (Pubitemid 39552518)
46. 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.
47. Wozniak DJ, Ohman DE (1994) Transcriptional analysis of the Pseudomonas aeruginosa genes algR, algB, and algD reveals a hierarchy of alginate gene expression which is modulated by algT. J Bacteriol 176: 6007-6014. (Pubitemid 24309938)
48. Rodriguez-Rojas A, Mena A, Martin S, Borrell N, Oliver A, et al. (2009) Inactivation of the hmgA gene of Pseudomonas aeruginosa leads to pyomelanin hyperproduction, stress resistance and increased persistence in chronic lung infection. Microbiology 155: 1050-1057.
49. Vallet-Gely I, Sharp JS, Dove SL (2007) Local and global regulators linking anaerobiosis to cupA fimbrial gene expression in Pseudomonas aeruginosa. J Bacteriol 189: 8667-8676. (Pubitemid 350210037)
50. Hossain MJ, Rahman Kh S, Terhune JS, Liles MR (2012) An outer membrane porin protein modulates phage susceptibility in Edwardsiella ictaluri. Microbiology 158: 474-487.
51. Randall-Hazelbauer L, Schwartz M (1973) Isolation of the bacteriophage lambda receptor from Escherichia coli. J Bacteriol 116: 1436-1446.
52. de Vries GE, Raymond CK, Ludwig RA (1984) Extension of bacteriophage lambda host range: selection, cloning, and characterization of a constitutive lambda receptor gene. Proc Natl Acad Sci U S A 81: 6080-6084. (Pubitemid 15219596)
53. Rau MH, Marvig RL, Ehrlich GD, Molin S, Jelsbak L (2012) Deletion and acquisition of genomic content during early stage adaptation of Pseudomonas aeruginosa to a human host environment. Environ Microbiol 14: 2200-2211.
54. Krylov SV, Kropinski AM, Pleteneva EA, Shaburova OV, Burkal'tseva MV, et al. (2012) Properties of the new D3-like Pseudomonas aeruginosa bacteriophage phiPMG1: genome structure and prospects for the use in phage therapy. Genetika 48: 1057-1067.
55. Brussow H, Hendrix RW (2002) Phage genomics: small is beautiful. Cell 108: 13-16. (Pubitemid 34137008)
56. Casjens SR (2005) Comparative genomics and evolution of the tailed-bacteriophages. Curr Opin Microbiol 8: 451-458.
57. Braid MD, Silhavy JL, Kitts CL, Cano RJ, Howe MM (2004) Complete genomic sequence of bacteriophage B3, a Mu-like phage of Pseudomonas aeruginosa . J Bacteriol 186: 6560-6574. (Pubitemid 39258139)
58. Juhala RJ, Ford ME, Duda RL, Youlton A, Hatfull GF, et al. (2000) Genomic sequences of bacteriophages HK97 and HK022: pervasive genetic mosaicism in the lambdoid bacteriophages. J Mol Biol 299: 27-51.