Lytic activity by temperate phages of Pseudomonas aeruginosa in long-term cystic fibrosis chronic lung infections

ISME Journal

Volumn 9, Issue 6, 2015, Pages 1391-1398

  James, Chloe E ^a,b   Davies, Emily V ^a   Fothergill, Joanne L ^a   Walshaw, Martin J ^c   Beale, Colin M ^d   Brockhurst, Michael A ^d   Winstanley, Craig ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b UNIVERSITY OF SALFORD   (United Kingdom)

^c LIVERPOOL HEART AND CHEST HOSPITAL   (United Kingdom)

^d UNIVERSITY OF YORK   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DISEASE; BACTERIUM; CORRELATION; INFECTIOUS DISEASE; LONG-TERM CHANGE; LYSIS; POLYMERASE CHAIN REACTION; POPULATION DENSITY; QUANTITATIVE ANALYSIS; RODENT;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA; RATTUS;

COMPLEMENT;

ANIMAL; CYSTIC FIBROSIS; DISEASE MODEL; HUMAN; LUNG; MICROBIOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; PROPHAGE; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; PSEUDOMONAS PHAGE; RESPIRATORY TRACT INFECTION; SPUTUM; VIROLOGY;

ANIMALS; COMPLEMENT SYSTEM PROTEINS; CYSTIC FIBROSIS; DISEASE MODELS, ANIMAL; HUMANS; LUNG; POLYMERASE CHAIN REACTION; PROPHAGES; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTIONS; PSEUDOMONAS PHAGES; RESPIRATORY TRACT INFECTIONS; SPUTUM;

EID: 84929655888     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2014.223     Document Type: Article

References (39)

1. Al-Aloul M, Crawley J,Winstanley C, Hart CA, Ledson MJ, Walshaw MJ. (2004). Increased morbidity associated with chronic infection by an epidemic Pseudomonas aeruginosa strain in CF patients. Thorax 59: 334-336.
2. Ashish A, Shaw M, Winstanley C, Ledson MJ, Walshaw MJ. (2012). Increasing resistance of the Liverpool epidemic strain (LES) of Pseudomonas aeruginosa (Psa) to antibiotics in cystic fibrosis (CF)- a cause for concern? J Cyst Fibros 11: 173-179.
3. Barr JJ, Auro R, Furlan M, Whiteson KL, Erb ML, Pogliano J et al. (2013). Bacteriophage adhering to mucus provide a non-host-derived immunity. Proc Natl Acad Sci USA 110: 10771-10776.
4. Bobay LM, Touchon M, Rocha EP. (2014). Pervasive domestication of defective prophages by bacteria. Proc Natl Acad Sci USA 111: 12127-12132.
5. Breitbart M, Hewson I, Felts B, Mahaffy JM, Nulton J, Salamon P et al. (2003). Metagenomic analyses of an uncultured viral community from human feces. J Bacteriol 185: 6220-6223.
6. 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.
7. Brussow H, Canchaya C, Hardt WD. (2004). Phages and the evolution of bacterial pathogens: from genomic rearrangements to lysogenic conversion. Microbiol Mol Biol Rev 68: 560-602.
8. Comeau AM, Tetart F, Trojet SN, Prere MF, Krisch HM. (2007). Phage-Antibiotic Synergy (PAS): beta-lactam and quinolone antibiotics stimulate virulent phage growth. PLoS One 2: e799.
9. Desiere F, McShan WM, van Sinderen D, Ferretti JJ, Brussow H. (2001). Comparative genomics reveals close genetic relationships between phages from dairy bacteria and pathogenic Streptococci: evolutionary implications for prophage-host interactions. Virology 288: 325-341.
10. Fodor AA, Klem ER, Gilpin DF, Elborn JS, Boucher RC, Tunney MM et al. (2012). The adult cystic fibrosis airway microbiota is stable over time and infection type, and highly resilient to antibiotic treatment of exacerbations. PLoS One 7: e45001.
11. Fothergill JL, Mowat E, Ledson MJ, Walshaw MJ, Winstanley C. (2010). Fluctuations in phenotypes and genotypes within populations of Pseudomonas aeruginosa in the cystic fibrosis lung during pulmonary exacerbations. J Med Microbiol 59: 472-481.
12. Fothergill JL, Mowat E, Walshaw MJ, Ledson MJ, James CE, Winstanley C. (2011). Effect of antibiotic treatment on bacteriophage production by a cystic fibrosis epidemic strain of Pseudomonas aeruginosa. Antimicrob Agents Chemother 55: 426-428.
13. Fothergill JL, Walshaw MJ, Winstanley C. (2012). Transmissible strains of Pseudomonas aeruginosa in Cystic Fibrosis lung infections. Eur Respir J 40: 227-238.
14. Fothergill JL, Ledson MJ, Walshaw MJ, McNamara PS, Southern KW, Winstanley C. (2013). Comparison of real time diagnostic chemistries to detect Pseudomonas aeruginosa in respiratory samples from cystic fibrosis patients. J Cyst Fibros 12: 675-681.
15. Fothergill JL, Neill DR, Loman N, Winstanley C, Kadioglu A. (2014). Pseudomonas aeruginosa adaptation in the nasopharyngeal reservoir leads to migration and persistence in the lungs. Nature Communications 5: 4780.
16. Foweraker J. (2009). Recent advances in the microbiology of respiratory tract infection in cystic fibrosis. Br Med Bull 89: 93-110.
17. Ghosh D, Roy K, Williamson KE, Srinivasiah S, Wommack KE, Radosevich M. (2009). Acyl-homoserine lactones can induce virus production in lysogenic bacteria: an alternative paradigm for prophage induction. Appl Environ Microbiol 75: 7142-7152.
18. Goss CH, Burns JL. (2007). Exacerbations in cystic fibrosis. 1: epidemiology and pathogenesis. Thorax 62: 360-367.
19. Hagens S, Habel A, Blasi U. (2006). Augmentation of the antimicrobial efficacy of antibiotics by filamentous phage. Microb Drug Resist 12: 164-168.
20. James CE, Stanley KN, Allison HE, Flint HJ, Stewart CS, Sharp RJ et al. (2001). Lytic and lysogenic infection of diverse Escherichia coli and Shigella strains with a verocytotoxigenic bacteriophage. Appl Environ Microbiol 67: 4335-4337.
21. James CE, Fothergill JL, Kalwij H, Hall AJ, Cottell J, Brockhurst MA et al. (2012). Differential infection properties of three inducible prophages from an epidemic strain of Pseudomonas aeruginosa. BMC Microbiol 12: 216.
22. Kim MS, Park EJ, Roh SW, Bae JW. (2011). Diversity and abundance of single-stranded DNA viruses in human feces. Appl Environ Microbiol 77: 8062-8070.
23. Knezevic P, Curcin S, Aleksic V, Petrusic M, Vlaski L. (2013). Phage-antibiotic synergism: a possible approach to combatting Pseudomonas aeruginosa. Res Microbiol 164: 55-60.
24. Lawrence JG, Hendrix RW, Casjens S. (2001). Where are the pseudogenes in bacterial genomes? Trends Microbiol 9: 535-540.
25. Letkiewicz S, Miedzybrodzki R, Klak M, Jonczyk E, Weber-Dabrowska B, Gorski A. (2010). The perspectives of the application of phage therapy in chronic bacterial prostatitis. FEMS Immunol Med Microbiol 60: 99-112.
26. Lim YW, Evangelista JS 3rd, Schmieder R, Bailey B, Haynes M, FurlanMet al. (2014). Clinical insights from metagenomic analysis of sputum samples from patients with cystic fibrosis. J Clin Microbiol 52: 425-437.
27. Little JW. (2005). Lysogeny, prophage induction and lysogenic conversion. In: Waldor MK, Friedman A, Adhya S (eds) Phages. ASM Press: Washington DC, pp 37-54.
28. Martin K, Baddal B, Mustafa N, Perry C, Underwood A, Constantidou C et al. (2013). Clusters of genetically similar isolates of Pseudomonas aeruginosa from multiple hospitals in the United Kingdom. J Med Microbiol 62: 988-1000.
29. Matsushiro A, Sato K, Miyamoto H, Yamamura T, Honda T. (1999). Induction of prophages of enterohemorrhagic Escherichia coli O157:H7 with norfloxacin. J Bacteriol 181: 2257-2260.
30. McCallum SJ, Corkill J, Gallagher M, Ledson MJ, Hart CA, Walshaw MJ. (2001). Superinfection with a transmissible strain of Pseudomonas aeruginosa in adults with cystic fibrosis chronically colonised by P aeruginosa. Lancet 358: 558-560.
31. McGrath LT, Mallon P, Dowey L, Silke B, McClean E, McDonnell M et al. (1999). Oxidative stress during acute respiratory exacerbations in cystic fibrosis. Thorax 54: 518-523.
32. Mowat E, Paterson S, Fothergill JL, Wright EA, Ledson MJ, Walshaw MJ et al. (2011). Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. Am J Respir Crit Care Med 183: 1674-1679.
33. Ojeniyi B, Birch-Andersen A, Mansa B, Rosdahl VT, Hoiby N. (1991). Morphology of Pseudomonas aeruginosa phages from the sputum of cystic fibrosis patients and from the phage typing set. APMIS 99: 925-930.
34. Pinheiro JC, Bates DM. (2000). Linear Mixed-Effects Models: Basic Concepts And Examples. Springer: New York.
35. Reyes A, Semenkovich NP, Whiteson K, Rohwer F, Gordon JI. (2012). Going viral: next-generation sequencing applied to phage populations in the human gut. Nat Rev Microbiol 10: 607-617.
36. Wagner PL, Acheson DW, Waldor MK. (2001). Human neutrophils and their products induce Shiga toxin production by enterohemorrhagic Escherichia coli. Infect Immun 69: 1934-1937.
37. Willner D, Furlan M, Haynes M, Schmieder R, Angly FE, Silva J et al. (2009). Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS One 4: e7370.
38. Winstanley C, Langille MG, Fothergill JL, Kukavica-Ibrulj I, Paradis-Bleau C, Sanschagrin F et al. (2009). Newly introduced genomic prophage islands are critical determinants of in vivo competitiveness in the Liverpool Epidemic Strain of Pseudomonas aeruginosa. Genome Res 19: 12-23.
39. Wright EA, Fothergill JL, Paterson S, Brockhurst MA, Winstanley C. (2013). Sub-inhibitory concentrations of some antibiotics can drive diversification of Pseudomonas aeruginosa populations in artificial sputum medium. BMC Microbiol 13: 170.