Back to the future: Evolving bacteriophages to increase their effectiveness against the pathogen Pseudomonas aeruginosa PAO1

Evolutionary Applications

Volumn 6, Issue 7, 2013, Pages 1054-1063

  Betts, Alex ^a   Vasse, Marie ^a   Kaltz, Oliver ^a   Hochberg, Michael E ^a,b  

^a INSTITUT DES SCIENCES DE L EVOLUTION   (France)

^b SANTA FE INSTITUTE   (United States)

Author keywords

Coevolution; Cross infection; Cystic fibrosis; Disinfection; Evolutionary engineering; Experimental evolution; Nosocomial; Phage therapy; Phage training; Resistance

Indexed keywords

EID: 84885773922     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12085     Document Type: Article

References (77)

1. Abedon, S. 2011. Phage therapy pharmacology: calculating phage dosing. Advances in Applied Microbiology 77:1-40.
2. Abedon, S. T. 2012. Spatial vulnerability: Bacterial arrangements, microcolonies, and biofilms as responses to low rather than high phage densities. Viruses 4:663-687.
3. Alemayehu, D., P. G. Casey, O. McAuliffe, C. M. Guinane, J. G. Martin, F. Shanahan, A. Coffey et al. 2012. Bacteriophages φ{symbol}MR299-2 and φ{symbol}NH-4 can eliminate Pseudomonas aeruginosa in the murine lung and on cystic fibrosis lung airway cells. mBio 3:e00029-12.
4. Babu, K. V. Y., V. Vijayanath, H. P. Niranjan, and M. R. Anitha 2011. Study of imipenem resistant metallo- beta-lactamase positive Pseudomonas aeruginosa from burns wound infections, environmental sources and impact of infection control measures in a burns care center. Journal of Pure and Applied Microbiology 5:695-703.
5. Blanquart, F., and S. Gandon 2013. Time-shift experiments and patterns of adaptation across time and space. Ecology Letters 16:31-38.
6. Brockhurst, M. A., A. Buckling, and P. B. Rainey 2005. The effect of a bacteriophage on diversification of the opportunistic bacterial pathogen, Pseudomonas aeruginosa. Proceedings of the Royal Society B-Biological Sciences 272:1385-1391.
7. Brockhurst, M. A., A. D. Morgan, A. Fenton, and A. Buckling 2007. Experimental coevolution with bacteria and phage: the Pseudomonas fluorescens-Phi2 model system. Infection Genetics and Evolution 7:547-552.
8. Buckling, A., and P. B. Rainey 2002. Antagonistic coevolution between a bacterium and a bacteriophage. Proceedings of the Royal Society of London Series B-Biological Sciences 269:931-936.
9. Buckling, A., Y. Wei, R. C. Massey, M. A. Brockhurst, and M. E. Hochberg 2006. Antagonistic coevolution with parasites increases the cost of host deleterious mutations. Proceedings of the Royal Society B-Biological Sciences 273:45-49.
10. Buckling, A., C. R. Maclean, M. A. Brockhurst, and N. Colegrave 2009. The beagle in a bottle. Nature 457:824-829.
11. Carlton, R. M. 1999. Phage therapy: past history and future prospects. Archivum Immunologiae et Therapiae Experimentalis 47:267-274.
12. Carvalho, C. M., B. W. Gannon, D. E. Halfhide, S. B. Santos, C. M. Hayes, J. M. Roe, and J. Azeredo 2010. The in vivo efficacy of two administration routes of a phage cocktail to reduce numbers of Campylobacter coli and Campylobacter jejuni in chickens. BMC Microbiology 10:232.
13. Ceyssens, P. J., R. Lavigne, W. Mattheus, A. Chibeu, K. Hertveldt, J. Mast, and J. Robben et al. 2006. Genomic analysis of Pseudomonas aeruginosa phages LKD16 and LKA1: establishment of the phi KMV subgroup within the T7 supergroup. Journal of Bacteriology 188:6924-6931.
14. Ceyssens, P. J., K. Miroshnikov, W. Mattheus, V. Krylov, J. Robben, J. P. Noben, and S. Vanderschraeghe et al. 2009. Comparative analysis of the widespread and conserved PB1-like viruses infecting Pseudomonas aeruginosa. Environmental Microbiology 11:2874-2883.
15. Ceyssens, P. J., A. Brabban, L. Rogge, M. S. Lewis, D. Pickard, D. Goulding, and G. Dougan et al. 2010. Molecular and physiological analysis of three Pseudomonas aeruginosa phages belonging to the "N4-like viruses". Virology 405:26-30.
16. Chan, B. K., and S. T. Abedon 2012. Phage therapy pharmacology: phage cocktails. Advances in Applied Microbiology 78:1-23.
17. Chapman-McQuiston, E., and X. Wu 2008. Stochastic receptor expression allows sensitive bacteria to evade phage attack. Part I: Experiments. Biophysical Journal 94:4525-4536.
18. Chastre, J., and J. Y. Fagon 2002. Ventilator-associated pneumonia. American Journal of Respiratory and Critical Care Medicine 165:867-903.
19. D'Costa, V. M., C. E. King, L. Kalan, M. Morar, W. W. Sung, C. Schwarz, D. Froese et al. 2011. Antibiotic resistance is ancient. Nature 477:457-461.
20. Debarbieux, L., D. Leduc, D. Maura, E. Morello, A. Criscuolo, O. Grossi, V. Balloy et al. 2010. Bacteriophages can treat and prevent Pseudomonas aeruginosa lung infections. Journal of Infectious Diseases 201:1096-1104.
21. Deredjian, A., C. Colinon, E. Brothier, S. Favre-Bonte, B. Cournoyer, and S. Nazaret 2011. Antibiotic and metal resistance among hospital and outdoor strains of Pseudomonas aeruginosa. Research in Microbiology 162:689-700.
22. Driscoll, J. A., S. L. Brody, and M. H. Kollef 2007. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs 67:351-368.
23. Ebert, D. 1998. Evolution - Experimental evolution of parasites. Science 282:1432-1435.
24. Escobar-Páramo, P., C. Gougat-Barbera, and M. E. Hochberg 2012. Evolutionary dynamics of separate and combined exposure of Pseudomonas fluorescens SBW25 to antibiotics and bacteriophage. Evolutionary Applications 5:583-592.
25. Gaba, S., and D. Ebert 2009. Time-shift experiments as a tool to study antagonistic coevolution. Trends in Ecology & Evolution 24:226-232.
26. Garneau, J. E., M. E. Dupuis, M. Villion, D. A. Romero, R. Barrangou, P. Boyaval, C. Fremaux et al. 2010. The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA. Nature 468:67-71.
27. Goddard, A. F., B. J. Staudinger, S. E. Dowd, A. Joshi-Datar, R. D. Wolcott, M. L. Aitken, C. L. Fligner et al. 2012. Direct sampling of cystic fibrosis lungs indicates that DNA-based analyses of upper-airway specimens can misrepresent lung microbiota. Proceedings of the National Academy of Sciences of the United States of America 109:13769-13774.
28. Gomes, M. Z. R., C. R. Machado, M. de Souza da Conceição, J. A. Ortega, S. M. F. M. Neves, M. C. da Silva Lourenço, and M. D. Asensi 2011. Outbreaks, persistence, and high mortality rates of multiresistant Pseudomonas aeruginosa infections in a hospital with AIDS-predominant admissions. Brazilian Journal of Infectious Diseases 15:312-322.
29. Hagens, S., and M. J. Loessner 2010. Bacteriophage for biocontrol of foodborne pathogens: calculations and considerations. Current Pharmaceutical Biotechnology 11:58-68.
30. Hall, A. R., P. D. Scanlan, A. D. Morgan, and A. Buckling 2011. Host-parasite coevolutionary arms races give way to fluctuating selection. Ecology Letters 14:635-642.
31. Hall, A. R., D. De Vos, V. Friman, J. Pirnay, and A. Buckling 2012. Effects of sequential and simultaneous application of bacteriophages on populations of Pseudomonas aeruginosa in vitro and in waxmoth larvae. Applied and Environmental Microbiology 78:5646-5652.
32. Harcombe, W. R., and J. J. Bull 2005. Impact of phages on two-species bacterial communities. Applied and Environmental Microbiology 71:5254-5259.
33. Hardalo, C., and S. C. Edberg 1997. Pseudomonas aeruginosa: assessment of risk from drinking water. Critical Reviews in Microbiology 23:47-75.
34. Harper, D., and M. Enright 2011. Bacteriophages for the treatment of Pseudomonas aeruginosa infections. Journal of Applied Microbiology 111:1-7.
35. Johnston, J. R. 2002. A comparison of antibiotic resistance in bacteria isolated from conventionally versus organically raised livestock. BIOS (Ocean Grove) 73:47-51.
36. Jones, R. N. 2010. Microbial etiologies of hospital-acquired bacterial pneumonia and ventilator-associated bacterial pneumonia. Clinical Infectious Diseases 51:81-87.
37. Khawaldeh, A., S. Morales, B. Dillon, Z. Alavidze, A. N. Ginn, L. Thomas, S. J. Chapman et al. 2011. Bacteriophage therapy for refractory Pseudomonas aeruginosa urinary tract infection. Journal of Medical Microbiology 60:1697-1700.
38. King, E. O., M. K. Ward, and D. E. Raney 1954. 2 Simple media for the demonstration of pyocyanin and Fluorescin. Journal of Laboratory and Clinical Medicine 44:301-307.
39. Koskella, B., D. M. Lin, A. Buckling, and J. N. Thompson 2012. The costs of evolving resistance in heterogeneous parasite environments. Proceedings of the Royal Society B: Biological Sciences 279:1896-1903.
40. Kutateladze, M., and R. Adamia 2010. Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends in Biotechnology 28:591-595.
41. Kutter, E., D. De Vos, G. Gvasalia, Z. Alavidze, L. Gogokhia, S. Kuhl, and S. T. Abedon 2009. Phage therapy in clinical practice: treatment of human infections. Current Pharmaceutical Biotechnology 11:69-86.
42. Kysela, D. T., and P. E. Turner 2007. Optimal bacteriophage mutation rates for phage therapy. Journal of Theoretical Biology 249:411-421.
43. Levin, B. R., and J. J. Bull 2004. Population and evolutionary dynamics of phage therapy. Nature Reviews Microbiology 2:166-173.
44. Li, X.-I., and H. Nikaido 2009. Efflux-mediated drug resistance in bacteria: an update. Drugs 69:1555-1623.
45. Loc-Carrillo, C., and S. Abedon 2011. Pros and cons of phage therapy. Bacteriophage 1:111-114.
46. Lohse, K., A. Gutierrez, and O. Kaltz 2006. Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata. Evolution 60:1177-1186.
47. Lopez Pascua, L., S. Gandon, and A. Buckling 2012. Abiotic heterogeneity drives parasite local adaptation in coevolving bacteria and phages. Journal of Evolutionary Biology 25:195.
48. Lu, T. K., and J. J. Collins 2009. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proceedings of the National Academy of Sciences 106:4629-4634.
49. Lu, T. K., and M. S. Koeris 2011. The next generation of bacteriophage therapy. Current Opinion in Microbiology 14:524-531.
50. Maura, D., E. Morello, L. du Merle, P. Bomme, C. Le Bouguénec, and L. Debarbieux. 2012. Intestinal colonization by enteroaggregative Escherichia coli supports long-term bacteriophage replication in mice. Environmental Microbiology 14:1844-1854.
51. Morello, E., E. Saussereau, D. Maura, M. Huerre, L. Touqui, and L. Debarbieux 2011. Pulmonary bacteriophage therapy on Pseudomonas aeruginosa cystic fibrosis strains: first steps towards treatment and prevention. PLoS ONE 6:e16963.
52. Mowat, E., S. Paterson, J. L. Fothergill, E. A. Wright, M. J. Ledson, M. J. Walshaw, M. A. Brockhurst et al. 2011. Pseudomonas aeruginosa population diversity and turnover in cystic fibrosis chronic infections. American Journal of Respiratory and Critical Care Medicine 183:1674-1679.
53. Nuismer, S. L., R. Gomulkiewicz, and B. J. Ridenhour 2010. When is correlation coevolution? American Naturalist 175:525-537.
54. Paterson, S., T. Vogwill, A. Buckling, R. Benmayor, A. J. Spiers, N. R. Thomson, M. Quail et al. 2010. Antagonistic coevolution accelerates molecular evolution. Nature 464:275-278.
55. Pires, D., S. Sillankorva, A. Faustino, and J. Azeredo 2011. Use of newly isolated phages for control of Pseudomonas aeruginosa PAO1 and ATCC 10145 biofilms. Research in Microbiology 162:798-806.
56. Pirnay, J. P., G. Verbeken, T. Rose, S. Jennes, M. Zizi, I. Huys, R. Lavigne et al. 2012. Introducing yesterday's phage therapy in today's medicine. Future Virology 7:379-390.
57. Poisot, T., P. H. Thrall, J. D. Bever, A. Nemri, and M. E. Hochberg 2011a. A conceptual framework for the evolution of ecological specialisation. Ecology Letters 14:841-851.
58. Poisot, T., Lepennetier, G., E. Martinez, J. Ramsayer, and M. E. Hochberg. 2011b. Resource availability affects the structure of a natural bacteria-bacteriophage community. Biology Letters 7:201-204.
59. Poisot, T., P. H. Thrall, and M. E. Hochberg 2012. Trophic network structure emerges through antagonistic coevolution in temporally varying environments. Proceedings of the Royal Society B-Biological Sciences 279:299-308.
60. Pouillot, F., H. Blois, and F. Iris 2010. Genetically engineered virulent phage banks in the detection and control of emergent pathogenic bacteria. Biosecur Bioterror 8:155-169.
61. Poullain, V., S. Gandon, M. A. Brockhurst, A. Buckling, and M. E. Hochberg 2008. The evolution of specificity in evolving and coevolving antagonistic interactions between a bacteria and its phage. Evolution 62:1-11.
62. RQIA 2012. Independent Review of Incidents of Pseudomonas aeruginosa Infection in Neonatal Units in Northern Ireland. RQIA, Belfast.
63. Rumbaugh, K. P., J. A. Griswold, B. H. Iglewski, and A. N. Hamood 1999. Contribution of quorum sensing to the virulence of Pseudomonas aeruginosa in burn wound infections. Infection and Immunity 67:5854-5862.
64. SAS 1996. SAS/STAT User's guide, Release 6.11. SAS Institute, Cary, NC.
65. ® 10. SAS Institute Inc., Cary, NC.
66. Scott, A. E., A. R. Timms, P. L. Connerton, C. Loc Carrillo, R. K. Adzfa, and I. F. Connerton 2007. Genome dynamics of Campylobacter jejuni in response to bacteriophage predation. PLoS Pathogens 3:e119.
67. Secher, I., I. Hermes, S. Pre, F. Carreau, and F. Bahuet 2005. Surgical wound infections due to Pseudomonas aeruginosa in orthopedic surgery. Medecine et Maladies Infectieuses 35:149-154.
68. Sicard, D., P. S. Pennings, C. Grandclement, J. Acosta, O. Kaltz, and J. A. Shykoff 2007. Specialization and local adaptation of a fungal parasite on two host plant species as revealed by two fitness traits. Evolution 61:27-41.
69. Strateva, T., and D. Yordanov 2009. Pseudomonas aeruginosa - a phenomenon of bacterial resistance. Journal of Medical Microbiology 58:1133-1148.
70. Summers, W. C. 2001. Bacteriophage therapy. Annual Review of Microbiology 55:437-451.
71. Toprak, E., A. Veres, J.-B. Michel, R. Chait, D. L. Hartl, and R. Kishony 2012. Evolutionary paths to antibiotic resistance under dynamically sustained drug selection. Nature Genetics 44:101-105.
72. Uchiyama, J., I. Takemura, M. Satoh, S.-I. Kato, T. Ujihara, K. Akechi, S. Matsuzaki et al. 2011. Improved adsorption of an Enterococcus faecalis bacteriophage Phi EF24C with a spontaneous point mutation. PLoS ONE 6:e26648.
73. Vale, P. F., and T. J. Little 2010. CRISPR-mediated phage resistance and the ghost of coevolution past. Proceedings of the Royal Society B-Biological Sciences 277:2097-2103.
74. Verma, V., K. Harjai, and S. Chhibber 2010. Structural changes induced by a lytic bacteriophage make ciprofloxacin effective against older biofilm of Klebsiella pneumoniae. Biofouling 26:729-737.
75. VinodKumar, C. S., S. Kalsurmath, K. G. Basavarajappa, and G. Naganuur 2010. Utility of bacteriophage as a bio-disinfectant. Journal of Pure and Applied Microbiology 4:667-673.
76. Weitz, J. S., T. Poisot, J. R. Meyer, C. O. Flores, S. Valverde, M. B. Sullivan, and M. E. Hochberg 2013. Phage-bacteria infection networks. Trends in Microbiology 21:82-91.
77. Zhang, Q. G., and A. Buckling 2012. Phages limit the evolution of bacterial antibiotic resistance in experimental microcosms. Evolutionary Applications 5:575-582.