Differential infection properties of three inducible prophages from an epidemic strain of Pseudomonas aeruginosa

BMC Microbiology

Volumn 12, Issue , 2012, Pages

  James, Chloe E ^a   Fothergill, Joanne L ^a   Kalwij, Hannah ^a   Hall, Amanda J ^a   Cottell, Jennifer ^a   Brockhurst, Michael A ^b   Winstanley, Craig ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Bacteriophage infection; Cystic fibrosis; Host range; Prophage induction; Pseudomonas aeruginosa; Type IV pili

Indexed keywords

NORFLOXACIN;

ARTICLE; BACTERIAL STRAIN; GENE TRANSFER; LYSOGENIZATION; NONHUMAN; PROPHAGE; PSEUDOMONAS AERUGINOSA;

ADULT; ANIMALS; ANTI-BACTERIAL AGENTS; CHILD; CHILD, PRESCHOOL; CYSTIC FIBROSIS; FIMBRIAE, BACTERIAL; HUMANS; LYSOGENY; NORFLOXACIN; PROPHAGES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; SIPHOVIRIDAE; TRANSDUCTION, GENETIC; VIRAL PLAQUE ASSAY; VIRUS ACTIVATION; VIRUS INTERNALIZATION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA; RATTUS; SIPHOVIRIDAE;

EID: 84866504626     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-12-216     Document Type: Article

References (56)

1. Pseudomonas aeruginosa: assessment of risk from drinking water. Hardalo C, Edberg SC, Crit Rev Microbiol 1997 23 47 75 10.3109/10408419709115130 9097014 (Pubitemid 27154591)
2. Complete genome sequence of Pseudomonas aeruginosa PA01, an opportunistic pathogen. Stover CK, Pham XQ, Erwin AL, Mizoguchi SD, Warrener P, Hickey MJ, Brinkman FS, Hufnagle WO, Kowalik DJ, Lagrou M, et al. Nature 2000 406 959 964 10.1038/35023079 10984043
3. Multiple bacterial species reside in chronic wounds: a longitudinal study. Gjodsbol K, Christensen JJ, Karlsmark T, Jorgensen B, Klein BM, Krogfelt KA, Int Wound J 2006 3 225 231 10.1111/j.1742-481X.2006.00159.x 16984578 (Pubitemid 44426701)
4. Colonization of burn wounds in Ain Shams University Burn Unit. Nasser S, Mabrouk A, Maher A, Burns 2003 29 229 233 10.1016/S0305-4179(02)00285-1 12706615 (Pubitemid 36434383)
5. Endogenous and exogenous infection with Pseudomonas aeruginosa in a burns unit. Chitkara YK, Feierabend TC, Int Surg 1981 66 237 240 6797982 (Pubitemid 12110653)
6. Pathogenicity of microbes associated with cystic fibrosis. Hutchison ML, Govan JR, Microbes Infect 1999 1 1005 1014 10.1016/S1286-4579(99)80518-8 10617932
7. Pseudomonas aeruginosa biofilms in cystic fibrosis. Hoiby N, Ciofu O, Bjarnsholt T, Future Microbiol 2010 5 1663 1674 10.2217/fmb.10.125 21133688
8. Pseudomonas aeruginosa biofilm infections in cystic fibrosis: insights into pathogenic processes and treatment strategies. Hassett DJ, Korfhagen TR, Irvin RT, Schurr MJ, Sauer K, Lau GW, Sutton MD, Yu H, Hoiby N, Expert Opin Ther Targets 2010 14 117 130 10.1517/14728220903454988 20055712
9. Transmissible strains of Pseudomonas aeruginosa in Cystic Fibrosis lung infections. Fothergill JL, Walshaw MJ, Winstanley C, Eur Respir J 2012 40 227 238 10.1183/09031936.00204411 22323572
10. Spread of beta-lactam-resistant Pseudomonas aeruginosa in a cystic fibrosis clinic. Cheng K, Smyth RL, Govan JR, Doherty C, Winstanley C, Denning N, Heaf DP, van Saene H, Hart CA, Lancet 1996 348 639 642 10.1016/S0140-6736(96) 05169-0 8782753 (Pubitemid 26293808)
11. Superinfection with a transmissible strain of Pseudomonas aeruginosa in adults with cystic fibrosis chronically colonised by P aeruginosa. McCallum SJ, Corkill J, Gallagher M, Ledson MJ, Hart CA, Walshaw MJ, Lancet 2001 358 558 560 10.1016/S0140-6736(01)05715-4 11520530 (Pubitemid 32772735)
12. Increased morbidity associated with chronic infection by an epidemic Pseudomonas aeruginosa strain in CF patients. Al-Aloul M, Crawley J, Winstanley C, Hart CA, Ledson MJ, Walshaw MJ, Thorax 2004 59 334 336 10.1136/thx.2003. 014258 15047956 (Pubitemid 38496753)
13. PCR-based detection of a cystic fibrosis epidemic strain of Pseudomonas aeruginosa. Panagea S, Winstanley C, Parsons YN, Walshaw MJ, Ledson MJ, Hart CA, Mol Diagn 2003 7 195 200 10.2165/00066982-200307030-00009 15068391 (Pubitemid 38533788)
14. Identification and characterization of transmissible Pseudomonas aeruginosa strains in cystic fibrosis patients in England and Wales. Scott FW, Pitt TL, J Med Microbiol 2004 53 609 615 10.1099/jmm.0.45620-0 15184530 (Pubitemid 38932357)
15. Infection with transmissible strains of Pseudomonas aeruginosa and clinical outcomes in adults with cystic fibrosis. Aaron SD, Vandemheen KL, Ramotar K, Giesbrecht-Lewis T, Tullis E, Freitag A, Paterson N, Jackson M, Lougheed MD, Dowson C, et al. JAMA 2010 304 2145 2153 10.1001/jama.2010.1665 21081727
16. Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa. Winstanley C, Langille MG, Fothergill JL, Kukavica-Ibrulj I, Paradis-Bleau C, Sanschagrin F, Thomson NR, Winsor GL, Quail MA, Lennard N, et al. Genome Res 2009 19 12 23 19047519
17. Comparative genomic analysis of 18 Pseudomonas aeruginosa bacteriophages. Kwan T, Liu J, Dubow M, Gros P, Pelletier J, J Bacteriol 2006 188 1184 1187 10.1128/JB.188.3.1184-1187.2006 16428425 (Pubitemid 43146437)
18. O-antigen conversion in Pseudomonas aeruginosa PAO1 by bacteriophage D3. Kuzio J, Kropinski AM, J Bacteriol 1983 155 203 212 6190794 (Pubitemid 13071973)
19. Insertion and replication of the Pseudomonas aeruginosa mutator phage D3112. Rehmat S, Shapiro JA, Mol Gen Genet 1983 192 416 423 10.1007/BF00392184 6318038 (Pubitemid 14176063)
20. Bacteriophages of Pseudomonas. Ceyssens PJ, Lavigne R, Future Microbiol 2010 5 1041 1055 10.2217/fmb.10.66 20632804
21. Lysogenic conversion in Pseudomonas aeruginosa. Holloway BW, Cooper GN, J Bacteriol 1962 84 1321 1324 13961373
22. Phage-conversion of cytotoxin production in Pseudomonas aeruginosa. Hayashi T, Baba T, Matsumoto H, Terawaki Y, Mol Microbiol 1990 4 1703 1709 10.1111/j.1365-2958.1990.tb00547.x 2127632
23. The biofilm life cycle and virulence of Pseudomonas aeruginosa are dependent on a filamentous prophage. Rice SA, Tan CH, Mikkelsen PJ, Kung V, Woo J, Tay M, Hauser A, McDougald D, Webb JS, Kjelleberg S, ISME J 2009 3 271 282 10.1038/ismej.2008.109 19005496
24. Effect of antibiotic treatment on bacteriophage production by a cystic fibrosis epidemic strain of Pseudomonas aeruginosa. Fothergill JL, Mowat E, Walshaw MJ, Ledson MJ, James CE, Winstanley C, Antimicrob Agents Chemother 2011 55 426 428 10.1128/AAC.01257-10 20974862
25. Fluctuations in phenotypes and genotypes within populations of Pseudomonas aeruginosa in the cystic fibrosis lung during pulmonary exacerbations. Fothergill JL, Mowat E, Ledson MJ, Walshaw MJ, Winstanley C, J Med Microbiol 2010 59 472 481 10.1099/jmm.0.015875-0 20019149
26. Morphology of Pseudomonas aeruginosa phages from the sputum of cystic fibrosis patients and from the phage typing set. An electron microscopy study. Ojeniyi B, Birch-Andersen A, Mansa B, Rosdahl VT, Hoiby N, APMIS 1991 99 925 930 10.1111/j.1699-0463.1991.tb01280.x 1930965
27. Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Brussow H, Canchaya C, Hardt WD, Microbiol Mol Biol Rev 2004 68 560 602 10.1128/MMBR.68.3.560-602.2004 15353570 (Pubitemid 39238283)
28. Population structure of Pseudomonas aeruginosa. Wiehlmann L, Wagner G, Cramer N, Siebert B, Gudowius P, Morales G, Kohler T, van Delden C, Weinel C, Slickers P, Tummler B, Proc Natl Acad Sci U S A 2007 104 8101 8106 10.1073/pnas.0609213104 17468398 (Pubitemid 47185882)
29. Prophage F116: evidence for extrachromosomal location in Pseudomonas aeruginosa strain PAO. Miller RV, Pemberton JM, Clark AJ, J Virol 1977 22 844 847 406425 (Pubitemid 8109642)
30. Within-host competition determines reproductive success of temperate bacteriophages. Refardt D, ISME J 2011 5 1451 1460 10.1038/ismej.2011.30 21412345
31. Nucleotide sequence of the immunity region of bacteriophage Mu. Priess H, Kamp D, Kahmann R, Brauer B, Delius H, Mol Gen Genet 1982 186 315 321 10.1007/BF00729448 6214696 (Pubitemid 13231973)
32. Inhibition of superinfection and the evolution of viral latency. Berngruber TW, Weissing FJ, Gandon S, J Virol 2010 84 10200 10208 10.1128/JVI.00865-10 20660193
33. Virulent Mutants of Temperate Phage-Mu-1. Vanvliet F, Couturier M, Desmet L, Faelen M, Toussaint A, Mol Gen Genet 1978 160 195 202 10.1007/BF00267481 (Pubitemid 8320144)
34. Fine Structure of a Genetic Region in Bacteriophage. Benzer S, Proc Natl Acad Sci U S A 1955 41 344 354 10.1073/pnas.41.6.344 16589677
35. Superinfection exclusion by P22 prophage in lysogens of Salmonella typhimurium. III. Failure of superinfecting phage DNA to enter sieA+ lysogens. Susskind MM, Botstein D, Wright A, Virology 1974 62 350 366 10.1016/0042- 6822(74)90398-5 4610992
36. Superinfection exclusion by lambda prophage in lysogens of Salmonella typhimurium. Susskind MM, Botstein D, Virology 1980 100 212 216 10.1016/0042-6822(80)90571-1 6444259 (Pubitemid 10177896)
37. Molecular genetics of bacteriophage P22. Susskind MM, Botstein D, Microbiol Rev 1978 42 385 413 353481 (Pubitemid 8378880)
38. Genome sequence comparison and superinfection between two related Pseudomonas aeruginosa phages, D3112 and MP22. Heo YJ, Chung IY, Choi KB, Lau GW, Cho YH, Microbiology 2007 153 2885 2895 10.1099/mic.0.2007/007260-0 17768233 (Pubitemid 47517052)
39. Ecology of microbial invasions: amplification allows virus carriers to invade more rapidly when rare. Brown SP, Le Chat L, De Paepe M, Taddei F, Curr Biol 2006 16 2048 2052 10.1016/j.cub.2006.08.089 17055985 (Pubitemid 44604450)
40. Characterization of the Pseudomonas aeruginosa pilus adhesin: confirmation that the pilin structural protein subunit contains a human epithelial cell-binding domain. Irvin RT, Doig P, Lee KK, Sastry PA, Paranchych W, Todd T, Hodges RS, Infect Immun 1989 57 3720 3726 2572560
41. Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. O'Toole GA, Kolter R, Mol Microbiol 1998 30 295 304 10.1046/j.1365-2958.1998.01062.x 9791175 (Pubitemid 28480181)
42. Type IV pili and twitching motility. Mattick JS, Annu Rev Microbiol 2002 56 289 314 10.1146/annurev.micro.56.012302.160938 12142488 (Pubitemid 35217457)
43. Characterization of a gene, pilU, required for twitching motility but not phage sensitivity in Pseudomonas aeruginosa. Whitchurch CB, Mattick JS, Mol Microbiol 1994 13 1079 1091 10.1111/j.1365-2958.1994.tb00499.x 7854122
44. The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa. Brockhurst MA, Buckling A, Rainey PB, Proc Biol Sci 2005 272 1385 1391 10.1098/rspb.2005.3086 16006335 (Pubitemid 41414722)
45. The adsorption of Pseudomonas aeruginosa bacteriophage phiKMV is dependent on expression regulation of type IV pili genes. Chibeu A, Ceyssens PJ, Hertveldt K, Volckaert G, Cornelis P, Matthijs S, Lavigne R, FEMS Microbiol Lett 2009 296 210 218 10.1111/j.1574-6968.2009.01640.x 19459952
46. Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Mowat E, Paterson S, Fothergill JL, Wright EA, Ledson MJ, Walshaw MJ, Brockhurst MA, Winstanley C, Am J Respir Crit Care Med 2011 183 1674 1679 10.1164/rccm.201009-1430OC 21297072
47. Competition and dispersal in Pseudomonas aeruginosa. Taylor TB, Buckling A, Am Nat 2010 176 83 89 10.1086/652995 20500040
48. Common virulence factors for bacterial pathogenicity in plants and animals. Rahme LG, Stevens EJ, Wolfort SF, Shao J, Tompkins RG, Ausubel FM, Science 1995 268 1899 1902 10.1126/science.7604262 7604262
49. A cystic fibrosis epidemic strain of Pseudomonas aeruginosa displays enhanced virulence and antimicrobial resistance. Salunkhe P, Smart CH, Morgan JA, Panagea S, Walshaw MJ, Hart CA, Geffers R, Tummler B, Winstanley C, J Bacteriol 2005 187 4908 4920 10.1128/JB.187.14.4908-4920.2005 15995206 (Pubitemid 40962208)
50. Impact of Pseudomonas aeruginosa genomic instability on the application of typing methods for chronic cystic fibrosis infections. Fothergill JL, White J, Foweraker JE, Walshaw MJ, Ledson MJ, Mahenthiralingam E, Winstanley C, J Clin Microbiol 2010 48 2053 2059 10.1128/JCM.00019-10 20410349
51. Genetic characterization indicates that a specific subpopulation of Pseudomonas aeruginosa is associated with keratitis infections. Stewart RM, Wiehlmann L, Ashelford KE, Preston SJ, Frimmersdorf E, Campbell BJ, Neal TJ, Hall N, Tuft S, Kaye SB, Winstanley C, J Clin Microbiol 2011 49 993 1003 10.1128/JCM.02036-10 21227987
52. Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. Mahenthiralingam E, Coenye T, Chung JW, Speert DP, Govan JR, Taylor P, Vandamme P, J Clin Microbiol 2000 38 910 913 10655415 (Pubitemid 30082711)
53. Immunity profiles of wild-type and recombinant shiga-like toxin-encoding bacteriophages and characterization of novel double lysogens. Allison HE, Sergeant MJ, James CE, Saunders JR, Smith DL, Sharp RJ, Marks TS, McCarthy AJ, Infect Immun 2003 71 3409 3418 10.1128/IAI.71.6.3409-3418.2003 12761125 (Pubitemid 36637569)
54. Basic electron microscopy of aquatic viruses. Ackermann H-W, Heldal M, Manual of Aquatic Viral Ecology American Society of Limnology and Oceanography, Inc, Wilhelm SW, Weinbauer MG, Suttle CA, Waco TX, 2010 182 192
55. Real-time reverse transcriptase-polymerase chain reaction (RT-PCR) for measurement of cytokine and growth factor mRNA expression with fluorogenic probes or SYBR Green I. Yin JL, Shackel NA, Zekry A, McGuinness PH, Richards C, Putten KV, McCaughan GW, Eris JM, Bishop GA, Immunol Cell Biol 2001 79 213 221 10.1046/j.1440-1711.2001.01002.x 11380673 (Pubitemid 32522168)
56. Detection of specific sequences among DNA fragments separated by gel electrophoresis. Southern EM, J Mol Biol 1975 98 503 517 10.1016/S0022-2836(75) 80083-0 1195397