Temporal variation in antibiotic environments slows down resistance evolution in pathogenic Pseudomonas aeruginosa

Evolutionary Applications

Volumn 8, Issue 10, 2015, Pages 945-955

  Roemhild, Roderich ^a   Barbosa, Camilo ^a   Beardmore, Robert E ^b   Jansen, Gunther ^a   Schulenburg, Hinrich ^a  

^a UNIVERSITY OF KIEL   (Germany)

^b UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

Pseudomonas aeruginosa; Antibiotic cycling; Antibiotic resistance; Collateral sensitivity; Experimental evolution; Sequential therapy; Temporal variation

Indexed keywords

EID: 84954384044     PISSN: 17524563     EISSN: 17524571     Source Type: Journal    
DOI: 10.1111/eva.12330     Document Type: Article

References (47)

1. Abel Zur Wiesch, P., R. Kouyos, S. Abel, W. Viechtbauer, and S. Bonhoeffer 2014. Cycling empirical antibiotic therapy in hospitals: meta-analysis and models. PLoS Pathogens 10:e1004225.
2. Alto, B. W., B. R. Wasik, N. M. Morales, and P. E. Turner 2013. Stochastic temperatures impede RNA virus adaptation. Evolution 67:969-979.
3. Andersson, D. I., and D. Hughes 2014. Microbiological effects of sublethal levels of antibiotics. Nature Reviews Microbiology 12:465-478.
4. Bennett, K. M., J. E. Scarborough, M. Sharpe, E. Dodds-Ashley, K. S. Kaye, T. Z. Hayward, and S. N. Vaslef 2007. Implementation of antibiotic rotation protocol improves antibiotic susceptibility profile in a surgical intensive care unit. Journal of Trauma 63:307-311.
5. Breidenstein, E. B. M., C. de la Fuente-Núñez, and R. E. W. Hancock 2011. Pseudomonas aeruginosa: all roads lead to resistance. Trends in Microbiology 19:419-426.
6. Buckling, A., M. A. Brockhurst, M. Travisano, and P. B. Rainey 2007. Experimental adaptation to high and low quality environments under different scales of temporal variation. Journal of Evolutionary Biology 20:296-300.
7. Cooper, T. F., and R. E. Lenski 2010. Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evolutionary Biology 10:11.
8. Damkiær, S., L. Yang, S. Molin, and L. Jelsbak 2013. Evolutionary remodeling of global regulatory networks during long-term bacterial adaptation to human hosts. Proceedings of the National Academy of Sciences 110:7766-7771.
9. Duncan, A. B., S. Fellous, E. Quillery, and O. Kaltz 2011. Adaptation of Paramecium caudatum to variable conditions of temperature stress. Research in Microbiology 162:939-944.
10. Ekstrom, C. 2014. MESS: Miscellaneous Esoteric Statistical Scripts. http://CRAN.R-project.org/package=MESS (accessed on 21 July 2015).
11. Fuentes-Hernandez, A., J. Plucain, F. Gori, R. Pena-Miller, C. Reding, G. Jansen, H. Schulenburg et al. 2015. Using a sequential regimen to eliminate bacteria at sublethal antibiotic dosages. PLoS Biology 13:e1002104.
12. Habets, M. G. J. L., and M. A. Brockhurst 2012. Therapeutic antimicrobial peptides may compromise natural immunity. Biology Letters 8:416-418.
13. Hede, K. 2014. Antibiotic resistance: an infectious arms race. Nature 509:S2-S3.
14. Hegreness, M., N. Shoresh, D. Damian, D. Hartl, and R. Kishony 2008. Accelerated evolution of resistance in multidrug environments. Proceedings of the National Academy of Sciences 105:13977-13981.
15. Hothorn, T., F. Bretz, and P. Westfall 2008. Simultaneous inference in general parametric models. Biometrical Journal 50:346-363.
16. Imamovic, L., and M. O. A. Sommer 2013. Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development. Science Translational Medicine 5:204ra132.
17. Jasmin, J.-N., and R. Kassen 2007. On the experimental evolution of specialization and diversity in heterogeneous environments. Ecology Letters 10:272-281.
18. Kassen, R. 2002. The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology 15:173-190.
19. Ketola, T., L. Mikonranta, J. Zhang, K. Saarinen, A.-M. Örmälä, V.-P. Friman, J. Mappes et al. 2013. Fluctuating temperature leads to evolution of thermal generalism and preadaptation to novel environments. Evolution 67:2936-2944.
20. Kim, S., T. D. Lieberman, and R. Kishony 2014. Alternating antibiotic treatments constrain evolutionary paths to multidrug resistance. Proceedings of the National Academy of Sciences 111:14494-14499.
21. Lazar, V., G. Pal Singh, R. Spohn, I. Nagy, B. Horvath, M. Hrtyan, R. Busa-Fekete et al. 2014. Bacterial evolution of antibiotic hypersensitivity. Molecular Systems Biology 9:700.
22. Lenski, R. E. 1997. The cost of antibiotic resistance - from the perspective of a bacterium. In D. J. C. Organizer, and J. Goode, eds. Ciba Foundation Symposium 207 - Antibiotic Resistance: Origins, Evolution, Selection and Spread, pp. 131-151. John Wiley & Sons, Ltd., Chichester.
23. Lofton, H., M. Pränting, E. Thulin, and D. I. Andersson 2013. Mechanisms and fitness costs of resistance to antimicrobial peptides LL-37, CNY100HL and wheat germ histones. PLoS ONE 8:e68875.
24. Martínez, J.-A., J.-M. Nicolás, F. Marco, J.-P. Horcajada, G. Garcia-Segarra, A. Trilla, C. Codina et al. 2006. Comparison of antimicrobial cycling and mixing strategies in two medical intensive care units. Critical Care Medicine 34:329-336.
25. Marvig, R. L., L. M. Sommer, S. Molin, and H. K. Johansen 2015. Convergent evolution and adaptation of Pseudomonas aeruginosa within patients with cystic fibrosis. Nature Genetics 47:57-64.
26. May, M. 2014. Drug development: time for teamwork. Nature 509:S4-S5.
27. Mongold, J. A., A. F. Bennett, and R. E. Lenski 1996. Evolutionary adaptation to temperature. IV. Adaptation of Escherichia coli at a niche boundary. Evolution 50:35.
28. Munck, C., H. K. Gumpert, A. I. N. Wallin, H. H. Wang, and M. O. A. Sommer 2014. Prediction of resistance development against drug combinations by collateral responses to component drugs. Science Translational Medicine 6:262ra156-ra262ra156.
29. Oz, T., A. Guvenek, S. Yildiz, E. Karaboga, Y. T. Tamer, N. Mumcuyan, V. B. Ozan et al. 2014. Strength of selection pressure is an important parameter contributing to the complexity of antibiotic resistance evolution. Molecular Biology and Evolution 31:2387-2401.
30. Pena-Miller, R., D. Laehnemann, G. Jansen, A. Fuentes-Hernandez, P. Rosenstiel, H. Schulenburg, and R. Beardmore 2013. When the most potent combination of antibiotics selects for the greatest bacterial load: the smile-frown transition. PLoS Biology 11:e1001540.
31. Perron, G. G., M. Zasloff, and G. Bell 2006. Experimental evolution of resistance to an antimicrobial peptide. Proceedings of the Royal Society B-Biological Sciences 273:251-256.
32. 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 B-Biological Sciences 274:2351-2356.
33. Pinheiro, J., D. Bates, S. DebRoy, and D. Sarkar, R Core Team 2013. nlme: Linear and Nonlinear Mixed Effects Models. http://CRAN.R-project.org/package=nlme (accessed on 6 May 2015).
34. Poole, K. 2001. Multidrug resistance in Gram-negative bacteria. Current Opinion in Microbiology 4:500-508.
35. Poole, K. 2011. Pseudomonas aeruginosa: resistance to the max. Frontiers in Microbiology 2:65.
36. R Core Team. 2014. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing.
37. Rahme, L. G., E. J. Stevens, S. F. Wolfort, J. Shao, R. G. Tompkins, and F. M. Ausubel 1995. Common virulence factors for bacterial pathogenicity in plants and animals. Science (New York, N.Y.) 268:1899-1902.
38. Raymond, D. P., S. J. Pelletier, T. D. Crabtree, T. G. Gleason, L. L. Hamm, T. L. Pruett, and R. G. Sawyer 2001. Impact of a rotating empiric antibiotic schedule on infectious mortality in an intensive care unit. Critical Care Medicine 29:1101-1108.
39. Sarraf-Yazdi, S., M. Sharpe, K. M. Bennett, T. L. Dotson, D. J. Anderson, and S. N. Vaslef 2012. A 9-year retrospective review of antibiotic cycling in a surgical intensive care unit. Journal of Surgical Research 176:e73-e78.
40. Schenk, M. F., S. Witte, M. L. M. Salverda, B. Koopmanschap, J. Krug, and J. A. G. M. de Visser 2015. Role of pleiotropy during adaptation of TEM-1 β-lactamase to two novel antibiotics. Evolutionary Applications 8:248-260.
41. Szybalski, W., and V. Bryson 1952. Genetic studies on microbial cross resistance to toxic agents I. Cross resistance of Escherichia coli to fifteen antibiotics. Journal of Bacteriology 64:489-499.
42. US Centers for Disease Control and Prevention 2013. Antibiotic Resistance Threats in the United States, 2013.
43. Wang, C. Y., J. S. Jerng, K. Y. Cheng, L. N. Lee, C. J. Yu, P. R. Hsueh, and P. C. Yang 2006. Pandrug-resistant Pseudomonas aeruginosa among hospitalised patients: clinical features, risk-factors and outcomes. Clinical Microbiology & Infection 12:63-68.
44. Wright, G. 2014. Perspective: synthetic biology revives antibiotics. Nature 509:S13-S13.
45. Zasloff, M. 2002. Antimicrobial peptides of multicellular organisms. Nature 415:389-395.
46. Zhong, S., A. Khodursky, D. E. Dykhuizen, and A. M. Dean 2004. Evolutionary genomics of ecological specialization. Proceedings of the National Academy of Sciences of the United States of America 101:11719-11724.
47. Zimmermann, H., D. Gerhard, T. Dingermann, and L. A. Hothorn 2010. Statistical aspects of design and validation of microtitre-plate-based linear and non-linear parallel in vitro bioassays. Biotechnology Journal 5:62-74.