Limits to compensatory adaptation and the persistence of antibiotic resistance in pathogenic bacteria

Evolution, Medicine and Public Health

Volumn 2015, Issue 1, 2015, Pages 4-12

  MacLean, R Craig ^a   Vogwill, Tom ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Antibiotic resistance; Clinical microbiology; Compensatory adaptation; Experimental evolution; Fitness cost

Indexed keywords

AMOXICILLIN; ANTIBIOTIC AGENT; RIFAMPICIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL METABOLISM; BACTERIAL MUTATION; BACTERIAL SURVIVAL; BACTERIUM ISOLATE; CHROMOSOME MUTATION; COMPENSATORY ADAPTATION; DRUG DESIGN; DRUG TREATMENT FAILURE; EVOLUTIONARY ADAPTATION; GENETIC DRIFT; HAEMOPHILUS INFECTION; HORIZONTAL GENE TRANSFER; HUMAN; LABORATORY TEST; NONHUMAN; ORGANISMAL INTERACTION; PRESCRIPTION; PRIORITY JOURNAL; REVERTANT; TUBERCULOSIS;

EID: 84955621185     PISSN: None     EISSN: 20506201     Source Type: Journal    
DOI: 10.1093/emph/eou032     Document Type: Article

References (78)

1. Andersson DI. The biological cost of mutational antibiotic resistance: any practical conclusions? Curr Opin Microbiol 2006;9:461-5.
2. Andersson DI, Hughes D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Microbiol 2010;8:260-71.
3. Baltrus DA. Exploring the costs of horizontal gene transfer. Trends Ecol Evol 2013;28:489-95.
4. MacLean RC, Hall AR, Perron GG et al. The population genetics of antibiotic resistance: integrating molecular mechanisms and treatment contexts. Nat Rev Genet 2010;11:405-14.
5. Levin BR, Perrot V, Walker N. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 2000;154:985-97.
6. Lipsitch M, Bergstrom CT, Levin BR. The epidemiology of antibiotic resistance in hospitals: paradoxes and prescriptions. Proc Natl Acad Sci U S A 2000;97:1938-43.
7. zur Wiesch PA, Kouyos R, Engelstädter J et al. Population biological principles of drug-resistance evolution in infectious diseases. Lancet Infect Dis 2011;11:236-47.
8. zur Wiesch PS, Engelstaedter J, Bonhoeffer S. Compensation of fitness costs and reversibility of antibiotic resistance mutations. Antimicrob Agents Chemother 2010;54:2085-95.
9. Tanaka MM, Valckenborgh F. Escaping an evolutionary lobster trap: drug resistance and compensatory mutation in a fluctuating environment. Evolution 2011;65:1376-87.
10. Schrag SJ, Perrot V. Reducing antibiotic resistance. Nature 1996;381:120-1.
11. Schrag SJ, Perrot V, Levin BR. Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc R Soc B Biol Sci 1997;264:1287-91.
12. Maisnier-Patin S, Berg OG, Liljas L et al. Compensatory adaptation to the deleterious effect of antibiotic resistance in Salmonella typhimurium. Mol Microbiol 2002;46:355-66.
13. Nagaev I, Bjorkman J, Andersson DI et al. Biological cost and compensatory evolution in fusidic acid-resistant Staphylococcus aureus. Mol Microbiol 2001;40:433-9.
14. Comas I, Borrell S, Roetzer A et al. Whole-genome sequencing of rifampicin-resistant Mycobacterium tuberculosis strains identifies compensatory mutations in RNA polymerase genes. Nat Genet 2012;44:106-10.
15. Farhat MR, Shapiro BJ, Kieser KJ et al. Genomic analysis identifies targets of convergent positive selection in drugresistant Mycobacterium tuberculosis. Nat Genet 2013;45: 1183-9.
16. de Vos M, Mueller B, Borrell S et al. Putative compensatory mutations in the rpoC gene of rifampin-resistant Mycobacterium tuberculosis are associated with ongoing transmission. Antimicrob Agents Chemother 2013;57: 827-32.
17. Costelloe C, Metcalfe C, Lovering A et al. Effect of antibiotic prescribing in primary care on antimicrobial resistance in individual patients: systematic review and meta-analysis. Br Med J 2010;340:c2096.
18. Malhotra-Kumar S, Lammens C, Coenen S et al. Effect of azithromycin and clarithromycin therapy on pharyngeal carriage of macrolide-resistant streptococci in healthy volunteers: a randomised, double-blind, placebo-controlled study. Lancet 2007;369:482-90.
19. Chung A, Perera R, Brueggemann AB et al. Effect of antibiotic prescribing on antibiotic resistance in individual children in primary care: prospective cohort study. Br Med J 2007;335:429.
20. Sun L, Klein EY, Laxminarayan R. Seasonality and temporal correlation between community antibiotic use and resistance in the United States. Clin Infect Dis 2012.
21. Dagan R, Barkai G, Givon-Lavi N et al. Seasonality of antibiotic- resistant Streptococcus pneumoniae that causes acute otitis media: a clue for an antibiotic-restriction policy? J Infect Dis 2008;197:1094-102.
22. Enne VI, Livermore DM, Stephens P et al. Persistence of sulphonamide resistance in Escherichia coli in the UK despite national prescribing restriction. Lancet 2001;357: 1325-8.
23. Sundqvist M, Geli P, Andersson DI et al. Little evidence for reversibility of trimethoprim resistance after a drastic reduction in trimethoprim use. J Antimicrob Chemother 2010;65:350-60.
24. Enne VI, Bennett PM, Livermore DM et al. Enhancement of host fitness by the sul2-coding plasmid p9123 in the absence of selective pressure. J Antimicrob Chemother 2004; 53:958-63.
25. Bell BG, Schellevis F, Stobberingh E et al. A systematic review and meta-analysis of the effects of antibiotic consumption on antibiotic resistance. BMC Infect Dis 2014;14:13.
26. Abdelraouf K, Kabbara S, Ledesma KR et al. Effect of multidrug resistance-conferring mutations on the fitness and virulence of Pseudomonas aeruginosa. J Antimicrob Chemother 2011;66:1311-7.
27. Bhatter P, Chatterjee A, D'Souza D et al. Estimating fitness by competition assays between drug susceptible and resistant Mycobacterium tuberculosis of predominant lineages in Mumbai, India. PLoS One 2012;7:e33507.
28. Corich L, Dolzani L, Tonin EA et al. Metallo-Beta- Lactamase expression confers an advantage to Pseudomonas aeruginosa isolates compared with other Beta-Lactam resistance mechanisms, favoring the prevalence of Metallo-Beta-Lactamase producers in a clinical environment. Microb. Drug Resist 2010;16, 223-30.
29. Davies AP, Billington OJ, Bannister BA et al. Comparison of fitness of two isolates of Mycobacterium tuberculosis, one of which had developed multi-drug resistance during the course of treatment. J Infect 2000;41:184-7.
30. Foucault M-L, Courvalin P, Grillot-Courvalin C. Fitness cost of VanA-type vancomycin resistance in methicillinresistant Staphylococcus aureus. Antimicrob Agents Chemother 2009;53:2354-9.
31. Gagneux S, Long CD, Small PM et al. The competitive cost of antibiotic resistance in Mycobacterium tuberculosis. Science 2006;312:1944-6.
32. Gillespie SH, Billington OJ, Breathnach A, McHugh TD. Multiple drug-resistant Mycobacterium tuberculosis: evidence for changing fitness following passage through human hosts. Microb Drug Resist 2002;8:2739.
33. Nielsen KL, Pedersen TM, Udekwu KI et al. Fitness cost: a bacteriological explanation for the demise of the first international methicillin-resistant Staphylococcus aureus epidemic. J Antimicrob Chemother 2012;67:1325-32.
34. O'Sullivan DM, McHugh TD, Gillespie SH. Mapping the fitness of Mycobacterium tuberculosis strains: a omplex picture. J Med Microbiol 2010;59:1533-5.
35. Sandegren L, Lindqvist A, Kahlmeter G, Andersson DI. Nitrofurantoin resistance mechanism and fitness cost in Escherichia coli. J Antimicrob Chemoth 2008;62:495-503.
36. Shorten RJ, McGregor AC, Platt S et al. When is an outbreak not an outbreak? Fit, divergent strains of Mycobacterium tuberculosis display independent evolution of drug resistance in a large London outbreak. J Antimicrob Chemother 2013;68:543-9.
37. Sun Z, Jiao X, Peng Q et al. Antibiotic resistance in Pseudomonas aeruginosa is associated with decreased fitness. Cell Physiol Biochem 2013;31:347-54.
38. von Groll A, Martin A, Stehr M et al. Fitness of Mycobacterium tuberculosis strains of the W-Beijing and non-W-Beijing genotype. PLoS One 2010;5:e10191.
39. Nielsen KL, Pedersen TM, Udekwu KI et al. Fitness cost: a bacteriological explanation for the demise of the first international methicillin-resistant Staphylococcus aureus epidemic. J Antimicrob Chemother 2012;67: 1325-32.
40. Wielgoss S, Barrick JE, Tenaillon O et al. Mutation rate inferred from synonymous substitutions in a long-term evolution experiment with Escherichia coli. G3 2011;1: 183-6.
41. Gifford DR, MacLean RC. Evolutionary reversals of antibtioic resistance in experimental populations of Pseudomonas aeruginosa. Evolution 2013;67:2973-81.
42. Hall AR, Griffiths VF, MacLean RC et al. Mutational neighbourhood and mutation supply rate constrain adaptation in Pseudomonas aeruginosa. Proc R Soc Lond B Biol Sci 2010;277:643-50.
43. Bjorkman J, Nagaev I, Berg OG et al. Effects of environment on compensatory mutations to ameliorate costs of antibiotic resistance. Science 2000;287:1479-82.
44. Meka VG, Gold HS, Cooke A et al. Reversionto susceptibility in a linezolid-resistant clinical isolateof Staphylococcus aureus. J Antimicrob Chemother 2004;54:818-20.
45. Phillips G, Funnell B. Plasmid Biology. Washington, D.C: ASM Press, 2004.
46. Smith J. The social evolution of bacterial pathogenesis. Proc R Soc Lond Biol Sci 2001;268:61-9.
47. Vogwill T, MacLean RC. The genetic basis of the fitness cost of antimicrobial resistance: a meta-anlysis approach. Evol Appl. 2015; (in press).
48. Drusano GL. Antimicrobial pharmacodynamics: critical interactions of 'bug and drug'. Nat Rev Microbiol 2004;2: 289-300.
49. Balaban NQ. Persistence: mechanisms for triggering and enhancing phenotypic variability. Curr Opin Genet Dev 2011;21:768-75.
50. Balaban NQ, Merrin J, Chait R et al. Bacterial persistence as a phenotypic switch. Science 2004;305:1622-5.
51. Javid B, Sorrentino F, Toosky M et al. Mycobacterial mistranslation is necessary and sufficient for rifampicin phenotypic resistance. Proc Natl Acad Sci U S A 2014; 111:1132-7.
52. Silander OK, Nikolic N, Zaslaver A et al. A genome-wide analysis of promoter-mediated phenotypic noise in Escherichia coli. PLoS Genet 2012;8:e1002443.
53. Avery SV. Microbial cell individuality and the underlying sources of heterogeneity. Nat Rev Microbiol 2006;4:577-87.
54. Sánchez-Romero MA, Casadesús J. Contribution of phenotypic heterogeneity to adaptive antibiotic resistance. Proc Natl Acad Sci U S A 2013;111:355-60.
55. Ni M, Decrulle AL, Fontaine F et al. Pre-disposition and epigenetics govern variation in bacterial survival upon stress. PLoS Genet 2012;8:e1003148.
56. Wakamoto Y, Dhar N, Chait R et al. Dynamic persistence of antibiotic-stressed Mycobacteria. Science 2013;339:91-5.
57. Zhang H, Li D, Zhao L et al. Genome sequencing of 161 Mycobacterium tuberculosis isolates from China identifies genes and intergenic regions associated with drug resistance. Nat Genet 2013;45:1255-60.
58. Brandis G, Wrande M, Liljas L et al. Fitness-compensatory mutations in rifampicin-resistant RNA polymerase. Mol Microbiol 2012;85:142-51.
59. Maisnier-Patin S, Andersson DI. Adaptation to the deleterious effects of antimicrobial drug resistance mutations by compensatory evolution. Res Microbiol 2004;155: 360-69.
60. Löfmark S, Jernberg C, Billström H et al. Restored fitness leads to long-term persistence of resistant Bacteroides strains in the human intestine. Anaerobe 2008;14:157-60.
61. Karami N, Hannoun C, Adlerberth I et al. Colonization dynamics of ampicillin-resistant Escherichia coli in the infantile colonic microbiota. J Antimicrob Chemother 2008; 62:703-8.
62. Sjölund M, Wreiber K, Andersson DI et al. Long-term persistence of resistant enterococcus species after antibiotics to eradicate Helicobacter pylori. Ann Intern Med 2003;139: 483-7.
63. World Health Organization. Antimicrobial resistance: global report on surveillance 2014. World Health Organization, 2014.
64. Kumarasamy KK, Toleman MA, Walsh TR et al. Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study. Lancet Infect Dis 2010;10:597-602.
65. Hawkey PM, Jones AM. The changing epidemiology of resistance. J Antimicrob Chemother 2009;64(Suppl 1), i3-10.
66. Alekshun MN, Levy SB. Molecular mechanisms of antibacterial multidrug resistance. Cell 2007;128:1037-50.
67. Levy SB, Marshall B. Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 2004;10: S122-9.
68. Carattoli A. Plasmids and the spread of resistance. Int J Med Microbiol 2013;303:298-304.
69. Harrison E, Brockhurst MA. Plasmid-mediated horizontal gene transfer is a coevolutionary process. Trends Microbiol 2012;20:262-7.
70. Millan AS, Penã-Miller R, Toll-Riera M et al. Positive selection and compensatory adaptation interact to stabilize non-transmissible plasmids. Nat Commun 2014;5:5208.
71. Bouma JE, Lenski RE. Evolution of a bacteria/plasmid association. Nature 1988;335:351-2.
72. Vogwill T, Kojadinovic M, Furió V et al. Testing the role of genetic background in parallel evolution using the comparative experimental evolution of antibiotic resistance. Mol Biol Evol 2014;31:3314-23.
73. Smith EE, Buckley DG, Wu Z et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci U S A 2006;103:8487-92.
74. Croucher NJ, Harris SR, Fraser C et al. Rapid pneumococcal evolution in response to clinical interventions. Science 2011;331:430-4.
75. Mwangi MM, Wu SW, Zhou Y et al. Tracking the in vivo evolution of multidrug resistance in Staphylococcus aureus by whole-genome sequencing. Proc Nat Acad Sci U S A 2007;104:9451-6.
76. Lieberman TD, Michel J-B, Aingaran M et al. Parallel bacterial evolution within multiple patients identifies candidate pathogenicity genes. Nat Genet 2011;43: 1275-80.
77. Young BC, Golubchik T, Batty EM et al. Evolutionary dynamics of Staphylococcus aureus during progression from carriage to disease. Proc Natl Acad Sci U S A 2012;109: 4550-5.
78. Marvig RL, Johansen HK, Molin S et al. Genome analysis of a transmissible lineage of Pseudomonas aeruginosa reveals pathoadaptive mutations and distinct evolutionary paths of hypermutators. PLoS Genet 2013;9: e1003741.