Exposure to phages has little impact on the evolution of bacterial antibiotic resistance on drug concentration gradients

Evolutionary Applications

Volumn 7, Issue 3, 2014, Pages 394-402

  Zhang, Quan Guo ^a  

^a BEIJING NORMAL UNIVERSITY   (China)

Author keywords

Competitive ability; Fitness costs; Growth rate; Mutation supply; Phage therapy; Resistance reversion

Indexed keywords

EID: 84897859487     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12136     Document Type: Article

References (63)

1. Andersson, D. I. 2006. The biological cost of mutational antibiotic resistance: any practical conclusions? Current Opinion in Microbiology 9:461-465.
2. Andersson, D. I., and D. Hughes 2011. Persistence of antibiotic resistance in bacterial populations. FEMS Microbiology Reviews 35:901-911.
3. Bailey, M. J., A. K. Lilley, I. P. Thompson, P. B. Rainey, and R. J. Ellis 1995. Site directed chromosomal marking of a fluorescent pseudomonad isolated from the phytosphere of sugar beet; Stability and potential for marker gene transfer. Molecular Ecology 4:755-763.
4. Baquero, F., and M. C. Negri 1997. Selective compartments for resistant microorganisms in antibiotic gradients. BioEssays 19:731-736.
5. Barrow, P. A., and J. S. Soothill 1997. Bacteriophage therapy and prophylaxis: rediscovery and renewed assessment of potential. Trends in Microbiology 5:268-271.
6. Bell, G. 2008. Selection: the Mechanism of Evolution. 2nd edn. Oxford University Press, Oxford.
7. Bohannan, B. J. M., and R. E. Lenski 2000. Linking genetic change to community evolution: insights from studies of bacteria and bacteriophage. Ecology Letters 3:362-377.
8. Bohannan, B. J. M., M. Travisano, and R. E. Lenski 1999. Epistatic interactions can lower the cost of resistance to multiple consumers. Evolution 53:292-295.
9. Brockhurst, M. A., A. D. Morgan, A. Fenton, and A. Buckling 2007. Experimental coevolution with bacteria and phage: the Pseudomonas fluorescens-Φ2 model system. Infection, Genetics and Evolution 7:547-552.
10. Brown, E. M., and D. Nathwani 2005. Antibiotic cycling or rotation: a systematic review of the evidence of efficacy. Journal of Antimicrobial Chemotherapy 55:6-9.
11. Buckling, A., and M. Brockhurst. 2012. Bacteria-virus coevolution. In O. S. Soyer ed. Evolutionary Systems Biology, pp. 347-370. Springer, New York.
12. 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.
13. 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 of London Series B-Biological Sciences 273:45-49.
14. Cairns, B. J., and R. J. H. Payne 2008. Bacteriophage therapy and the mutant selection window. Antimicrobial Agents and Chemotherapy 52:4344-4350.
15. Cantón, R., and M.-I. Morosini 2011. Emergence and spread of antibiotic resistance following exposure to antibiotics. FEMS Microbiology Reviews 35:977-991.
16. Chanishvili, N., T. Chanishvili, M. Tediashvili, and P. A. Barrow 2001. Phages and their application against drug-resistant bacteria. Journal of Chemical Technology and Biotechnology 76:689-699.
17. Chopra, I., A. J. O'Neill, and K. Miller 2003. The role of mutators in the emergence of antibiotic-resistant bacteria. Drug Resistance Update 6:137-145.
18. Couce, A., and J. Blazquez 2009. Side effects of antibiotics on genetic variability. FEMS Microbiology Reviews 33:531-538.
19. Crawley, M. 2007. The R book. John Wiley & Sons Ltd, Chichester.
20. Elliott, A. M., S. E. Berning, M. D. Iseman, and C. A. Peloquin 1995. Failure of drug penetration and acquisition of drug-resistance in chronic tuberculous empyema. Tubercle and Lung Disease 76:463-467.
21. Enne, V. I., A. A. Delsol, J. M. Roe, and P. M. Bennett 2004. Rifampicin resistance and its fitness cost in Enterococcus faecium. Journal of Antimicrobial Chemotherapy 53:203-207.
22. 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.
23. Fantin, B., X. Duval, L. Massias, L. Alavoine, F. Chau, S. Retout, A. Andremont et al. 2009. Ciprofloxacin dosage and emergence of resistance in human commensal bacteria. Journal of Infectious Diseases 200:390-398.
24. Forde, S. E., J. N. Thompson, R. D. Holt, and B. J. M. Bohannan 2008. Coevolution drives temporal changes in fitness and diversity across environments in a bacteria-bacteriophage interaction. Evolution 62:1830-1839.
25. Gagneux, S., C. D. Long, P. M. Small, T. Van, G. K. Schoolnik, and B. J. M. Bohannan 2006. The competitive cost of antibiotic resistance in Mycobacterium tuberculosis. Science 312:1944-1946.
26. Greulich, P., B. Waclaw, and R. J. Allen 2012. Mutational pathway determines whether drug gradients accelerate evolution of drug-resistant cells. Physical Review Letters 109:088101.
27. Habets, M. G. J. L., and M. A. Brockhurst 2012. Therapeutic antimicrobial peptides may compromise natural immunity. Biology Letters 8:416-418.
28. Harrison, E., A.-L. Laine, M. Hietala, and M. A. Brockhurst 2013. Rapidly fluctuating environments constrain coevolutionary arms races by impeding selective sweeps. Proceedings of the Royal Society of London Series B-Biological Sciences 280:20130937.
29. Henrichfreise, B., I. Wiegand, I. Luhmer-Becker, and B. Wiedemann 2007. Development of resistance in wild-type and hypermutable Pseudomonas aeruginosa strains exposed to clinical pharmacokinetic profiles of meropenem and ceftazidime simulated in vitro. Antimicrobial Agents and Chemotherapy 51:3642-3649.
30. Hermsen, R., J. B. Deris, and T. Hwa 2012. On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient. Proceedings of the National Academy of Sciences of the United States of America 109:10775-10780.
31. Kohanski, M. A., M. A. DePristo, and J. J. Collins 2010. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Molecular Cell 37:311-320.
32. 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 of London Series B-Biological Sciences 279:1896-1903.
33. Kutateladze, M., and R. Adamia 2010. Bacteriophages as potential new therapeutics to replace or supplement antibiotics. Trends in Biotechnology 28:591-595.
34. Kutter, E., D. De Vos, G. Gvasalia, Z. Alavidze, L. Gogokhia, S. Kuhl, and S. T. Abedon 2010. Phage therapy in clinical practice: treatment of human infections. Current Pharmaceutical Biotechnology 11:69-86.
35. Lenski, R. E., M. R. Rose, S. C. Simpson, and S. C. Tadler 1991. Long-term experimental evolution in Escherichia coli. I. adaptation and divergence during 2, 000 generations. American Naturalist 138:1315-1341.
36. Levin, B. R., and J. J. Bull 1996. Phage therapy revisited: the population biology of a bacterial infection and its treatment with bacteriophage and antibiotics. American Naturalist 147:881-898.
37. Levin, B. R., V. Perrot, and N. Walker 2000. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154:985-997.
38. Lopez-Pascua, L. D. C., and A. Buckling 2008. Increasing productivity accelerates host-parasite coevolution. Journal of Evolutionary Biology 21:853-860.
39. Lozovsky, E. R., T. Chookajorn, K. M. Brown, M. Imwong, P. J. Shaw, S. Kamchonwongpaisan, D. E. Neafsey et al. 2009. Stepwise acquisition of pyrimethamine resistance in the malaria parasite. Proceedings of the National Academy of Sciences of the United States of America 106:12025-12030.
40. MacLean, R. C., A. R. Hall, G. G. Perron, and A. Buckling 2010. The population genetics of antibiotic resistance: integrating molecular mechanisms and treatment contexts. Nature Reviews Genetics 11:405-414.
41. Maisnier-Patin, S., O. G. Berg, L. Liljas, and D. I. Andersson 2002. Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Molecular Microbiology 46:355-366.
42. Masterton, R. G. 2005. Antibiotic cycling: more than it might seem? Journal of Antimicrobial Chemotherapy 55:1-5.
43. Monk, A. B., C. D. Rees, P. Barrow, S. Hagens, and D. R. Harper 2010. Bacteriophage applications: where are we now? Letters in Applied Microbiology 51:363-369.
44. Morgan, A. D., S. G. Gandon, and A. Buckling 2005. The effect of migration on local adaptation in a coevolving host-parasite system. Nature 437:253-256.
45. Mouton, J. W., U. Theuretzbacher, W. A. Craig, P. M. Tulkens, H. Derendorf, and O. Cars 2008. Tissue concentrations: do we ever learn? Journal of Antimicrobial Chemotherapy 61:235-237.
46. Olofsson, S. K., P. Geli, D. I. Andersson, and O. Cars 2005. Pharmacodynamic model to describe the concentration-dependent selection of cefotaxime-resistant Escherichia coli. Antimicrobial Agents and Chemotherapy 49:5081-5091.
47. Perron, G. G., M. Zasloff, and G. Bell 2006. Experimental evolution of resistance to an antimicrobial peptide. Proceedings of the Royal Society of London Series B-Biological Sciences 273:251-256.
48. Perron, G. G., A. Gonzalez, and A. Buckling 2007. Source-sink dynamics shape the evolution of antibiotic resistance and its pleiotropic fitness cost. Proceedings of the Royal Society of London Series B-Biological Sciences 274:2351-2356.
49. Perron, G. G., A. Hall, and A. Buckling 2010. Hypermutability and compensatory adaptation in antibiotic-resistant bacteria. American Naturalist 176:303-311.
50. Pirnay, J.-P., D. De Vos, G. Verbeken, M. Merabishvili, N. Chanishvili, M. Vaneechoutte, M. Zizi et al. 2011. The phage therapy paradigm: pret-a-porter or sur-mesure? Pharmaceutical Research 28:934-937.
51. R Development Core Team 2011. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
52. Rainey, P. B., and M. J. Bailey 1996. Physical and genetic map of the Pseudomonas fluorescens SBW25 chromosome. Molecular Microbiology 19:521-533.
53. Read, A. F., and S. Huijben 2009. Evolutionary biology and the avoidance of antimicrobial resistance. Evolutionary Applications 2:40-51.
54. Read, A. F., T. Day, and S. Huijben 2011. The evolution of drug resistance and the curious orthodoxy of aggressive chemotherapy. Proceedings of the National Academy of Sciences of the United States of America 108:10871-10877.
55. Schrag, S. J., V. Perrot, and B. R. Levin 1997. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proceedings of the Royal Society of London Series B-Biological Sciences 264:1287-1291.
56. Summers, W. C. 2001. Bacteriophage therapy. Annual Review of Microbiology 55:437-451.
57. Thiel, K. 2004. Old dogma, new tricks - 21st century phage therapy. Nature Biotechnology 22:31-36.
58. 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-U140.
59. Vogwill, T., A. Fenton, and M. A. Brockhurst 2009. Dispersal and natural enemies interact to drive spatial synchrony and decrease stability in patchy populations. Ecology Letters 12:1194-1200.
60. Ward, H., G. G. Perron, and R. C. Maclean 2009. The cost of multiple drug resistance in Pseudomonas aeruginosa. Journal of Evolutionary Biology 22:997-1003.
61. Weigand, M. R., and G. W. Sundin 2012. General and inducible hypermutation facilitate parallel adaptation in Pseudomonas aeruginosa despite divergent mutation spectra. Proceedings of the National Academy of Sciences of the United States of America 109:13680-13685.
62. Weinreich, D. M., N. F. Delaney, M. A. DePristo, and D. L. Hartl 2006. Darwinian evolution can follow only very few mutational paths to fitter proteins. Science 312:111-114.
63. Zhang, Q.-G., and A. Buckling 2012. Phages limit the evolution of bacterial antibiotic resistance in experimental microcosms. Evolutionary Applications 5:575-582.