Environmental and genetic modulation of the phenotypic expression of antibiotic resistance

FEMS Microbiology Reviews

Volumn 41, Issue 3, 2017, Pages 374-391

  Hughes, Diarmaid ^a   Andersson, Dan I ^a  

^a UPPSALA UNIVERSITY   (Sweden)

Author keywords

Epistasis; Heteroresistance; Pan genome; Persisters; Successful clones; Virulence

Indexed keywords

ANTIBIOTIC RESISTANCE; BACTERIOLOGY; DISSOCIATION; DNA SEQUENCE; EPISTASIS; GENE EXPRESSION; GENE MUTATION; GENETICS; GENOTYPE; IN VITRO STUDY; MODULATION; VIRULENCE; ADAPTATION; BACTERIUM; BIOFILM; DRUG EFFECTS; ENVIRONMENT; GROWTH, DEVELOPMENT AND AGING; HORIZONTAL GENE TRANSFER; HUMAN; MULTIDRUG RESISTANCE; MUTATION; PHENOTYPE; PHYSIOLOGY;

ANTIINFECTIVE AGENT;

ADAPTATION, PHYSIOLOGICAL; ANTI-BACTERIAL AGENTS; BACTERIA; BIOFILMS; DRUG RESISTANCE, MULTIPLE, BACTERIAL; ENVIRONMENT; GENE TRANSFER, HORIZONTAL; GENOTYPE; HUMANS; MUTATION; PHENOTYPE;

EID: 85020175478     PISSN: 01686445     EISSN: 15746976     Source Type: Journal    
DOI: 10.1093/femsre/fux004     Document Type: Review

References (227)

1. Abranches J, Martinez AR, Kajfasz JK et al. The molecular alarmone (p)ppGpp mediates stress responses, vancomycin tolerance, and virulence in Enterococcus faecalis. J Bacteriol 2009;191:2248-56
2. Accogli M, Giani T, Monaco M et al. Emergence of Escherichia coli ST131 sub-clone H30 producing VIM-1 and KPC-3 carbapenemases, Italy. J Antimicrob Chemoth 2014; 69:2293-6
3. Adler M, Anjum M, Andersson DI et al. Influence of acquired β-lactamases on the evolution of spontaneous carbapenem resistance in Escherichia coli. J Antimicrob Chemoth 2012; 68:51-9
4. Adriaenssens N, Coenen S, Versporten A et al. European Surveillance of Antimicrobial Consumption (ESAC): outpatient quinolone use in Europe (1997-2009). J Antimicrob Chemoth 2011;66:47-56
5. Alexander HE, Leidy G. Mode of action of streptomycin on type b hemophilus influenzae: II. Nature of resistant variants. J Exp Med 1947;85:607-21
6. Allison KR, Brynildsen MP, Collins JJ. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 2011;473:216-20
7. Anderson P, Roth J. Spontaneous tandem genetic duplications in Salmonella typhimurium arise by unequal recombination between rRNA (rrn) cistrons. P Natl Acad Sci USA 1981;78:3113-7
8. Andersson DI, Hughes D. Gene amplification and adaptive evolution in bacteria. Annu Rev Genet 2009;43:167-95
9. Andersson DI, Hughes D. Microbiological effects of sublethal levels of antibiotics. Nat Rev 2014;12:465-78
10. Andersson DI, Hughes D, Kubicek-Sutherland JZ. Mechanisms and consequences of bacterial resistance to antimicrobial peptides. Drug Resist Update 2016;26:43-57
11. Aziz RK, Kotb M. Rise and persistence of global M1T1 clone of Streptococcus pyogenes. Emerg Infect Dis 2008;14:1511-7
12. Banerjee R, Johnson JR. A new clone sweeps clean: the enigmatic emergence of Escherichia coli sequence type 131. Antimicrob Agents Ch 2014;58:4997-5004
13. Banerjee R, Robicsek A, Kuskowski MA et al. Molecular epidemiology of Escherichia coli sequence type 131 and Its H30 and H30-Rx subclones among extended-spectrum-beta lactamase-positive and-negative E. coli clinical isolates from the Chicago Region, 2007 to 2010. Antimicrob Agents Ch 2013;57:6385-8
14. Bauer ME, Shafer WM. On the in vivo significance of bacterial resistance to antimicrobial peptides. Biochim Biophys Acta 2015;1848:3101-11
15. Bernier SP, Lebeaux D, DeFrancesco AS et al. Starvation, together with the SOS response, mediates high biofilmspecific tolerance to the fluoroquinolone ofloxacin. PLoS Genet 2013;9:e1003144
16. Bjarnsholt T, Jensen PO, Burmolle M et al. Pseudomonas aeruginosa tolerance to tobramycin, hydrogen peroxide and polymorphonuclear leukocytes is quorum-sensing dependent. Microbiology 2005;151:373-83
17. Bonnin RA, Poirel L, Carattoli A et al. Characterization of an IncFII plasmid encoding NDM-1 from Escherichia coli ST131. PLoS One 2012;7:e34752
18. Borrell S, Teo Y, Giardina F et al. Epistasis between antibiotic resistance mutations drives the evolution of extensively drugresistant tuberculosis. Evol Med Public Health 2013;2013:65-74
19. Borriello G, Werner E, Roe F et al. Oxygen limitation contributes to antibiotic tolerance of Pseudomonas aeruginosa in biofilms. Antimicrob Agents Ch 2004;48:2659-64
20. Brandis G, Hughes D. Genetic characterization of compensatory evolution in strains carrying rpoB Ser531Leu, the rifampicin resistance mutation most frequently found in clinical isolates. J Antimicrob Chemoth 2013;68:2493-7
21. Brandis G, Pietsch F, Alemayehu R et al. Comprehensive phenotypic characterization of rifampicin resistance mutations in Salmonella provides insight into the evolution of resistance in Mycobacterium tuberculosis. J Antimicrob Chemoth 2015;70:680-5
22. Brandis G, Wrande M, Liljas L et al. Fitness-compensatory mutations in rifampicin-resistant RNA polymerase. Mol Microbiol 2012;85:142-51
23. Brook I. The role of beta-lactamase-producing-bacteria in mixed infections. BMC Infect Dis 2009;9:202
24. Brueggemann AB, Pai R, Crook DWet al. Vaccine escape recombinants emerge after pneumococcal vaccination in the United States. PLoS Pathog 2007;3:e168
25. Brueggemann AB, Peto TE, Crook DW et al. Temporal and geographic stability of the serogroup-specific invasive disease potential of Streptococcus pneumoniae in children. J Infect Dis 2004;190:1203-11
26. Bush K. Proliferation and significance of clinically relevant betalactamases. Ann NY Acad Sci 2013;1277:84-90
27. Cai JC, Zhang R, Hu YY et al. Emergence of Escherichia coli sequence type 131 isolates producing KPC-2 carbapenemase in China. Antimicrob Agents Ch 2014;58:1146-52
28. Casali N, Nikolayevskyy V, Balabanova Y et al. Microevolution of extensively drug-resistant tuberculosis in Russia. Genome Res 2012;22:735-45
29. Ceri H, Olson ME, Stremick C et al. The Calgary Biofilm Device: newtechnology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J Clin Microbiol 1999;37:1771-6
30. Chancey ST, Zahner D, Stephens DS. Acquired inducible antimicrobial resistance in Gram-positive bacteria. Future Microbiol 2012;7:959-78
31. Chancey ST, Zhou XL, Zahner D et al. Induction of effluxmediated macrolide resistance in Streptococcus pneumoniae. Antimicrob Agents Ch 2011;55:3413-22
32. Chen L, Mathema B, Chavda KD et al. Carbapenemase-producing Klebsiella pneumoniae: molecular and genetic decoding. Trends Microbiol 2014;22:686-96
33. Chen L, Mathema B, Pitout JD et al. Epidemic Klebsiella pneumoniae ST258 is a hybrid strain. MBio 2014; 5:e01355-01314
34. Chi F, Nolte O, Bergmann C et al. Crossing the barrier: Evolution and spread of a major class of mosaic pbp2x in Streptococcus pneumoniae, S-mitis and S-oralis. Int J Med Microbiol 2007;297:503-12
35. Chiang WC, Nilsson M, Jensen PO et al. Extracellular DNA shields against aminoglycosides in Pseudomonas aeruginosa biofilms. Antimicrob Agents Ch 2013;57:2352-61
36. Ciofu O, Tolker-Nielsen T, Jensen PO et al. Antimicrobial resistance, respiratory tract infections and role of biofilms in lung infections in cystic fibrosis patients. Adv Drug Deliver Rev 2015;85:7-23
37. Clancy CJ, Chen L, Hong JH et al. Mutations of the ompK36 porin gene and promoter impact responses of sequence type 258, KPC-2-producing Klebsiella pneumoniae strains to doripenem and doripenem-colistin. Antimicrob Agents Ch 2013;57:5258-65
38. Cohen R, Biscardi S, Levy C. The multifaceted impact of pneumococcal conjugate vaccine implementation in children in France between 2001 to 2014. Hum Vacc Immunother 2016;12:277-84
39. Cohen SP, Levy SB, Foulds J et al. Salicylate induction of antibiotic-resistance in Escherichia coli-activation of the mar operon and a mar-independent pathway. J Bacteriol 1993;175:7856-62
40. Cole JN, Barnett TC, Nizet V et al. Molecular insight into invasive group A streptococcal disease. Nat Rev 2011;9:724-36
41. 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
42. Cooke FJ, Brown DJ, Fookes M et al. Characterization of the genomes of a diverse collection of Salmonella enterica serovar Typhimurium definitive phage type 104. J Bacteriol 2008;190:8155-62
43. Coque TM, Novais A, Carattoli A et al. Dissemination of clonally related Escherichia coli strains expressing extendedspectrum beta-lactamase CTX-M-15. Emerg Infect Dis 2008;14:195-200
44. Cramer N, Wiehlmann L, Tummler B. Clonal epidemiology of Pseudomonas aeruginosa in cystic fibrosis. Int J Med Microbiol 2010;300:526-33
45. Croxen MA, Finlay BB. Molecular mechanisms of Escherichia coli pathogenicity. Nat Rev Microbiol 2010;8:26-38
46. Cubillos-Ruiz A, Morales J, Zambrano MM. Analysis of the genetic variation in Mycobacterium tuberculosis strains by multiple genome alignments. BMC Res Notes 2008;1:110
47. D'Costa VM, McGrann KM, Hughes DW et al. Sampling the antibiotic resistome. Science 2006;311:374-7
48. Dar D, Shamir M, Mellin JR et al. Term-seq reveals abundant ribo-regulation of antibiotics resistance in bacteria. Science 2016;352: aad9822
49. Dautzenberg MJ, Haverkate MR, Bonten MJ et al. Epidemic potential of Escherichia coli ST131 and Klebsiella pneumoniae ST258: a systematic reviewand meta-analysis. BMJ Open 2016;6:e009971
50. Delcour AH. Outer membrane permeability and antibiotic resistance. BBA-Proteins Proteom 2009;1794:808-16
51. Deleo FR, Chen L, Porcella SF et al. Molecular dissection of the evolution of carbapenem-resistant multilocus sequence type 258 Klebsiella pneumoniae. P Natl Acad Sci USA 2014;111:4988-93
52. Depardieu F, Podglajen I, Leclercq R et al. Modes and modulations of antibiotic resistance gene expression. Clin Microbiol Rev 2007;20:79-114
53. Doublet B, Boyd D, Mulvey MR et al. The Salmonella genomic island 1 is an integrative mobilizable element. Mol Microbiol 2005;55:1911-24
54. Dowson CG, Coffey TJ, Kell C et al. Evolution of penicillin resistance in Streptococcus pneumonia-the role of Streptococcus mitis in the formation of a low-affinity Pbp2b in Streptococcus pneumoniae. Mol Microbiol 1993;9:635-43
55. Durao P, Trindade S, Sousa A et al. Multiple resistance at no cost: rifampicin and streptomycin a dangerous liaison in the spread of antibiotic resistance. Mol Biol Evol 2015;32:2675-80
56. Dwyer DJ, Belenky PA, Yang JH et al. Antibiotics induce redoxrelated physiological alterations as part of their lethality. P Natl Acad Sci USA 2014;111:E2100-9
57. El-Halfawy OM, Valvano MA. Antimicrobial heteroresistance: an emerging field in need of clarity. Clin Microbiol Rev 2015;28:191-207
58. Eldholm V, Balloux F. Antimicrobial resistance in Mycobacterium tuberculosis: the odd one out. Trends Microbiol 2016;24:637-48
59. Fothergill JL, Walshaw MJ, Winstanley C. Transmissible strains of Pseudomonas aeruginosa in cystic fibrosis lung infections. Eur Respir J 2012;40:227-38
60. Foucault ML, Depardieu F, Courvalin P et al. Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci. P Natl Acad Sci USA 2010;107:16964-9
61. Geno KA, Gilbert GL, Song JY et al. Pneumococcal capsules and their types: past, present, and future. Clin Microbiol Rev 2015;28:871-99
62. Georgiou G, Shuler ML, Wilson DB. Release of periplasmic enzymes and other physiological effects of betalactamase overproduction in Escherichia coli. Biotechnol Bioeng 1988;32:741-8
63. Gillis RJ, White KG, Choi KH et al. Molecular basis of azithromycin-resistant Pseudomonas aeruginosa biofilms. Antimicrob Agents Ch 2005;49:3858-67
64. Ginsberg AM. Drugs in development for tuberculosis. Drugs 2010;70:2201-14
65. Girgis HS, Harris K, Tavazoie S. Large mutational target size for rapid emergence of bacterial persistence. P Natl Acad Sci USA 2012;109:12740-5
66. Gomes DM, Ward KE, LaPlante KL. Clinical implications of vancomycin heteroresistant and intermediately susceptible Staphylococcus aureus. Pharmacotherapy 2015;35:424-32
67. Gooderham WJ, Hancock RE. Regulation of virulence and antibiotic resistance by two-component regulatory systems in Pseudomonas aeruginosa. FEMS Microbiol Rev 2009;33:279-94
68. Gullberg E, Cao S, Berg OG et al. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 2011;7:e1002158
69. Hakenbeck R, Bruckner R, Denapaite D et al. Molecular mechanisms of beta-lactam resistance in Streptococcus pneumoniae. Future Microbiol 2012;7:395-410
70. Hall AR, MacLean RC. Epistasis buffers the fitness effects of rifampicin-resistance mutations in Pseudomonas aeruginosa. Evolution 2011;65:2370-9
71. Hanson ND, Sanders CC. Regulation of inducible AmpC betalactamase expression among Enterobacteriaceae. Curr Pharm Des 1999;5:881-94
72. Hatherell HA, Colijn C, Stagg HR et al. Interpreting whole genome sequencing for investigating tuberculosis transmission: a systematic review. BMC Med 2016;14:21
73. Helling RB, Janes BK, Kimball H et al. Toxic waste disposal in Escherichia coli. J Bacteriol 2002;184:3699-703
74. Henriques-Normark B, Blomberg C, Dagerhamn J et al. The rise and fall of bacterial clones: Streptococcus pneumoniae. Nat Rev 2008;6:827-37
75. Hicks LA, Harrison LH, Flannery B et al. Incidence of pneumococcal disease due to non-pneumococcal conjugate vaccine (PCV7) serotypes in the United States during the era of widespread PCV7 vaccination, 1998-2004. J Infect Dis 2007;196:1346-54
76. Hilty M, Betsch BY, Bogli-Stuber K et al. Transmission dynamics of extended-spectrum beta-lactamase-producing Enterobacteriaceae in the tertiary care hospital and the household setting. Clin Infect Dis 2012;55:967-75
77. Hirakawa H, Nishino K, Yamada J et al. Beta-lactam resistance modulated by the overexpression of response regulators of two-component signal transduction systems in Escherichia coli. J Antimicrob Chemoth 2003;52:576-82
78. Hjort K, Nicoloff H, Andersson DI. Unstable tandem gene amplification generates heteroresistance (variation in resistance within a population) to colistin in Salmonella enterica. Mol Microbiol 2016;102:274-89
79. Hoiby N, Bjarnsholt T, Givskov M et al. Antibiotic resistance of bacterial biofilms. Int J Antimicrob Ag 2010;35:322-32
80. Hooper DC. Mechanisms of fluoroquinolone resistance. Drug Resist Update 1999;2:38-55
81. Hooper DC. Mechanisms of action of antimicrobials: focus on fluoroquinolones. Clin Infect Dis 2001;32 ( Suppl 1):S9-15
82. Hooper DC, Wolfson JS, Ng EY et al. Mechanisms of action of and resistance to ciprofloxacin. Am J Med 1987;82:12-20
83. Horinouchi S, Weisblum B. Posttranscriptional modification of messenger-RNA conformation-mechanism that regulates erythromycin-induced resistance. P Natl Acad Sci-Biol 1980;77:7079-83
84. Hornsey M, Ellington MJ, Doumith M et al. Emergence of AcrABmediated tigecycline resistance in a clinical isolate of Enterobacter cloacae during ciprofloxacin treatment. Int J Antimicrob Agents 2010;35:478-81
85. Hughes D, Andersson DI. Selection of resistance at lethal and non-lethal antibiotic concentrations. Curr Opin Microbiol 2012;15:555-60
86. Huseby DL, Pietsch F, Brandis G et al. Mutation supply and relative fitness shape the genotypes of ciprofloxacinresistant Escherichia coli. Mol Biol Evol 2017, doi: 10.1093/molbev/msx1052
87. Ito A, Taniuchi A, May T et al. Increased antibiotic resistance of Escherichia coli in mature biofilms. Appl Environ Microb 2009;75:4093-100
88. Ito M, Deguchi T, Mizutani KS et al. Emergence and spread of Neisseria gonorrhoeae clinical isolates harboring mosaiclike structure of penicillin-binding protein 2 in central Japan. Antimicrob Agents Ch 2005;49:137-43
89. Jacoby GA. AmpC beta-lactamases. Clin Microbiol Rev 2009;22:161-82
90. Jacoby GA. Mechanisms of resistance to quinolones. Clin Infect Dis 2005;41 ( Suppl 2):S120-6
91. Johnsborg O, Eldholm V, Bjornstad ML et al. A predatory mechanism dramatically increases the efficiency of lateral gene transfer in Streptococcus pneumoniae and related commensal species. Mol Microbiol 2008;69:245-53
92. Johnson JR, Miller S, Johnston B et al. Sharing of Escherichia coli sequence type ST131 and other multidrug-resistant and Urovirulent E. coli strains among dogs and cats within a household. J Clin Microbiol 2009;47:3721-5
93. Johnson JR, Tchesnokova V, Johnston B et al. Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli. J Infect Dis 2013;207:919-28
94. Johnson SR, Grad Y, Ganakammal SR et al. In vitro selection of Neisseria gonorrhoeae mutants with elevated MIC values and increased resistance to cephalosporins. Antimicrob Agents Ch 2014;58:6986-9
95. Johnson TJ, Hargreaves M, Shaw K et al. Complete genome sequence of a carbapenem-resistant extraintestinal pathogenic Escherichia coli strain belonging to the sequence type 131 H30R subclade. Genome Announc 2015;3:e00272-00215
96. Jolivet-Gougeon A, Bonnaure-MalletM. Biofilms as a mechanism of bacterial resistance. Drug Discov Today Technol 2014;11:49-56
97. Kayser FH, Benner EJ, Hoeprich PD. Acquired and native resistance of Staphylococcus aureus to cephalexin and other beta-lactam antibiotics. Appl Microbiol 1970;20:1-5
98. Keren I, Wu YX, Inocencio J et al. Killing by bactericidal antibiotics does not depend on reactive oxygen species. Science 2013;339:1213-6
99. Kester JC, Fortune SM. Persisters and beyond: Mechanisms of phenotypic drug resistance and drug tolerance in bacteria. Crit Rev Biochem Mol 2014;49:91-101
100. Kim L, McGee L, Tomczyk S et al. Biological and epidemiological features of antibiotic-resistant Streptococcus pneumoniae in pre-and post-conjugate vaccine eras: a United States Perspective. Clin Microbiol Rev 2016;29:525-52
101. Kohanski MA, Dwyer DJ, Hayete B et al. A common mechanism of cellular death induced by bactericidal antibiotics. Cell 2007;130:797-810
102. Kolpen M, Mousavi N, Sams T et al. Reinforcement of the bactericidal effect of ciprofloxacin on Pseudomonas aeruginosa biofilm by hyperbaric oxygen treatment. Int J Antimicrob Ag 2016;47:163-7
103. Komp Lindgren P, Karlsson Å, Hughes D. Mutation rate and evolution of fluoroquinolone resistance in Escherichia coli isolates from patients with urinary tract infections. Antimicrob Agents Ch 2003;47:3222-32
104. KompLindgren P, Marcusson LL, Sandvang D et al. Biological cost of single and multiple norfloxacin resistance mutations in Escherichia coli implicated in urinary tract infections. Antimicrob Agents Ch 2005;49:2343-51
105. Koskiniemi S, Pranting M, Gullberg E et al. Activation of cryptic aminoglycoside resistance in Salmonella enterica. MolMicrobiol 2011;80:1464-78
106. Koul A, Arnoult E, Lounis N et al. The challenge of new drug discovery for tuberculosis. Nature 2011;469:483-90
107. Kubicek-Sutherland JZ, Heithoff DM, Ersoy SC et al. Hostdependent induction of transient antibiotic resistance: a prelude to treatment failure. Ebiomedicine 2015; 2:1169-78
108. Kwon AR, Min YH, Yoon EJ et al. ermK leader peptide: amino acid sequence critical for induction by erythromycin. Arch Pharm Res 2006;29:1154-7
109. LaRock CN, Dohrmann S, Todd J et al. Group A streptococcal M1 protein sequesters cathelicidin to evade innate immune killing. Cell Host Microbe 2015;18:471-7
110. Le Bouter A, Leclercq R, Cattoir V. Molecular basis of resistance to macrolides, lincosamides and streptogramins in Staphylococcus saprophyticus clinical isolates. Int J Antimicrob Ag 2011;37:118-23
111. Lederberg J, Zinder N. Concentration of biochemical mutants of bacteria with penicillin. J Am Chem Soc 1948;70:4267
112. Lee SW, Foley EJ, Epstein JA. Mode of action of penicillin l Bacterial growth and penicillin activity-Staphylococcus aureus FDA. J Bacteriol 1944;48:393-9
113. Lee Y, Kim BS, Chun J et al. Clonality and Resistome analysis of KPC-producing Klebsiella pneumoniae strain isolated in Korea using whole genome sequencing. Biomed Res Int 2014;2014:352862
114. Leekitcharoenphon P, Hendriksen RS, Le Hello S et al. Global Genomic Epidemiology of Salmonella enterica Serovar Typhimurium DT104. Appl Environ Microb 2016;82:2516-26
115. Levin BR, Concepcion-Acevedo J, Udekwu KI. Persistence: a copacetic and parsimonious hypothesis for the existence of non-inherited resistance to antibiotics. Curr Opin Microbiol 2014;21:18-21
116. Levin BR, Rozen DE. Non-inherited antibiotic resistance. Nat Rev 2006;4:556-62
117. Li XZ, Plesiat P, Nikaido H. The challenge of efflux-mediated antibiotic resistance in Gram-negative bacteria. Clin Microbiol Rev 2015;28:337-418
118. Liao J, Sauer K. The MerR-like transcriptional regulator BrlR contributes to Pseudomonas aeruginosa biofilm tolerance. J Bacteriol 2012;194:4823-36
119. Liao J, Schurr MJ, Sauer K. The MerR-like regulator BrlR confers biofilm tolerance by activating multidrug efflux pumps in Pseudomonas aeruginosa biofilms. J Bacteriol 2013;195:3352-63
120. Lioy VS, Goussard S, Guerineau V et al. Aminoglycoside resistance 16S rRNA methyltransferases block endogenous methylation, affect translation efficiency and fitness of the host. RNA 2014;20:382-91
121. Liu Y, Wan LG, Deng Q et al. First description of NDM-1-, KPC-2-, VIM-2-and IMP-4-producing Klebsiella pneumoniae strains in a single Chinese teaching hospital. Epidemiol Infect 2015;143:376-84
122. Liu YY, Imlay JA. Cell death from antibiotics without the involvement of reactive oxygen species. Science 2013;339:1210-3
123. Lobritz MA, Belenky P, Porter CBM et al. Antibiotic efficacy is linked to bacterial cellular respiration. P Natl Acad Sci USA 2015;112:8173-80
124. Loftie-Eaton W, Yano H, Burleigh S et al. Evolutionary paths that expand plasmid host range: implications for spread of antibiotic resistance. Mol Biol Evol 2016;33:885-97
125. Lynch SV, Dixon L, Benoit MR et al. Role of the rapA gene in controlling antibiotic resistance of Escherichia coli biofilms. Antimicrob Agents Ch 2007;51:3650-8
126. McCallum SJ, Gallagher MJ, Corkill JE et al. Spread of an epidemic Pseudomonas aeruginosa strain from a patient with cystic fibrosis (CF) to non-CF relatives. Thorax 2002;57:559-60
127. McCollister BD, Hoffman M, Husain M et al. Nitric oxide protects bacteria from aminoglycosides by blocking the energydependent phases of drug uptake. Antimicrob Agents Ch 2011;55:2189-96
128. Mckay SL, Portnoy DA. Ribosome hibernation facilitates tolerance of stationary-phase bacteria to Aminoglycosides. Antimicrob Agents Ch 2015;59:6992-9
129. Maddocks JL, May JR. Indirect pathogenicity of penicillinaseproducing enterobacteria in chronic bronchial infections. Lancet 1969;1:793-5
130. Mah TF, Pitts B, Pellock B et al. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 2003;426:306-10
131. Maiden MC. Horizontal genetic exchange, evolution, and spread of antibiotic resistance in bacteria. Clin Infect Dis 1998;27 (Suppl 1):S12-20
132. Marcusson LL, Frimodt-Moller N, Hughes D. Interplay in the selection of fluoroquinolone resistance and bacterial fitness. PLoS Pathog 2009;5:e1000541
133. Martinez-Martinez L, Pascual A, Jacoby GA. Quinolone resistance from a transferable plasmid. Lancet 1998;351:797-9
134. Matamouros S, Miller SI. S. Typhimurium strategies to resist killing by cationic antimicrobial peptides. BBA-Biomembranes 2015;1848:3021-5
135. Mathers AJ, Peirano G, Pitout JD. Escherichia coli ST131: The quintessential example of an international multiresistant high-risk clone. Adv Appl Microbiol 2015;90:109-54
136. Mathers AJ, Peirano G, Pitout JD. The role of epidemic resistance plasmids and international high-risk clones in the spread of multidrug-resistant Enterobacteriaceae. Clin Microbiol Rev 2015;28:565-91
137. Matiasovicova J, Adams P, Barrow PA et al. Identification of putative ancestors of themultidrug-resistant Salmonella enterica serovar typhimurium DT104 clone harboring the Salmonella genomic island 1. Arch Microbiol 2007;187:415-24
138. Mayer C, Takiff H. The molecular genetics of fluoroquinolone resistance in Mycobacterium tuberculosis. Microbiol Spectr 2014;2: MGM2-0009-2013
139. Mayford M, Weisblum B. Ermc leader peptide-amino-acid sequence critical for induction by translational attenuation. J Mol Biol 1989;206:69-79
140. Mishra R, Shukla P, Huang W et al. Gene mutations in Mycobacterium tuberculosis: multidrug-resistant TB as an emerging global public health crisis. Tuberculosis (Edinb) 2015;95:1-5
141. Morosini MI, Ayala JA, Baquero F et al. Biological cost of AmpC production for Salmonella enterica serotype Typhimurium. Antimicrob Agents Ch 2000;44:3137-43
142. Mortimer PG, Piddock LJ. The accumulation of five antibacterial agents in porin-deficient mutants of Escherichia coli. J Antimicrob Chemoth 1993;32:195-213
143. Moyed HS, Bertrand KP. hipA, a newly recognized gene of Escherichia coli K-12 that affects frequency of persistence after inhibition of murein synthesis. J Bacteriol 1983;155:768-75
144. Naas T, Cuzon G, Gaillot O et al. When carbapenem-hydrolyzing beta-lactamase Kpc meets Escherichia coli ST131 in France. Antimicrob Agents Ch 2011;55:4933-4
145. Naseer U, Haldorsen B, Tofteland S et al. Molecular characterization of CTX-M-15-producing clinical isolates of Escherichia coli reveals the spread ofmultidrug-resistant ST131 (O25:H4) and ST964 (O102:H6) strains in Norway. APMIS 2009;117:526-36
146. Nasser W, Beres SB, Olsen RJ et al. Evolutionary pathway to increased virulence and epidemic group A Streptococcus disease derived from 3, 615 genome sequences. P Natl Acad Sci USA 2014;111:E1768-76
147. Nebenzahl-Guimaraes H, Jacobson KR, Farhat MR et al. Systematic review of allelic exchange experiments aimed at identifying mutations that confer drug resistance in Mycobacterium tuberculosis. J Antimicrob Chemoth 2014;69:331-42
148. Negri MC, Lipsitch M, Blazquez J et al. Concentration-dependent selection of small phenotypic differences in TEM betalactamase-mediated antibiotic resistance. Antimicrob Agents Ch 2000;44:2485-91
149. Nemeth J, Oesch G, Kuster SP. Bacteriostatic versus bactericidal antibiotics for patients with serious bacterial infections: systematic review and meta-analysis. J Antimicrob Chemoth 2015;70:382-95
150. Nicolas-Chanoine MH, Bertrand X, Madec JY. Escherichia coli ST131, an intriguing clonal group. Clin Microbiol Rev 2014;27:543-74
151. Nicolas-Chanoine MH, Blanco J, Leflon-Guibout V et al. Intercontinental emergence of Escherichia coli clone O25: H4-ST131 producing CTX-M-15. J Antimicrob Chemoth 2008;61:273-81
152. Nicolle LE. Pivmecillinam in the treatment of urinary tract infections. J Antimicrob Chemoth 2000;46:35-39
153. Nicoloff H, Andersson DI. Indirect resistance to several classes of antibiotics in cocultures with resistant bacteria expressing antibiotic-modifying or-degrading enzymes. J Antimicrob Chemoth 2016;71:100-10
154. Nishino K, Hayashi-Nishino M, Yamaguchi A. H-NS modulatesmultidrug resistance of Salmonella enterica serovar Typhimurium by repressing multidrug efflux genes acrEF. Antimicrob Agents Ch 2009;53:3541-3
155. Nordmann P, Cuzon G, Naas T. The real threat of Klebsiella pneumoniae carbapenemase-producing bacteria. Lancet Infect Dis 2009;9:228-36
156. Novais A, Viana D, Baquero F et al. Contribution of IncFII and broad-host IncA/C and IncN plasmids to the local expansion and diversification of phylogroup B2 Escherichia coli ST131 clones carrying bla(CTX-M-15) and qnrS1 genes. Antimicrob Agents Ch 2012;56:2763-6
157. O'Hara JA, Hu F, Ahn C et al. Molecular epidemiology of KPC-producing Escherichia coli: occurrence of ST131-fimH30 subclone harboring pKpQIL-like IncFIIk plasmid. Antimicrob Agents Ch 2014;58:4234-7
158. Ochiai S, Ishiko H, Yasuda M et al. Rapid detection of the mosaic structure of the Neisseria gonorrhoeae penA gene, which is associated with decreased susceptibilities to oral cephalosporins. J Clin Microbiol 2008;46:1804-10
159. Ojo KK, Striplin MJ, Ulep CC et al. Staphylococcus efflux msr(A) gene characterized in Streptococcus, Enterococcus, Corynebacterium, and Pseudomonas isolates. Antimicrob Agents Ch 2006;50:1089-91
160. Oliver A, Mulet X, Lopez-Causape C et al. The increasing threat of Pseudomonas aeruginosa high-risk clones. Drug Resist Update 2015;21-22:41-59
161. Olsen I. Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol 2015;34:877-86
162. Ortega A, Saez D, Bautista V et al. Carbapenemase-producing Escherichia coli is becoming more prevalent in Spain mainly because of the polyclonal dissemination of OXA-48. J Antimicrob Chemoth 2016;71:2131-8
163. Overdevest I, Haverkate M, Veenemans J et al. Prolonged colonisation with Escherichia coli O25:ST131 versus other extended-spectrum beta-lactamase-producing E. coli in a long-term care facility with high endemic level of rectal colonisation, the Netherlands, 2013 to 2014. Euro Surveill 2016;21:30376
164. Page R, Peti W. Toxin-antitoxin systems in bacterial growth arrest and persistence. Nat Chem Biol 2016;12:208-14
165. Partridge SR, Ellem JA, Tetu SG et al. Complete sequence of pJIE143, a pir-type plasmid carrying ISEcp1-bla(CTX-M-15) from an Escherichia coli ST131 isolate. Antimicrob Agents Ch 2011;55:5933-5
166. Pawlowski AC, Wang W, Koteva K et al. A diverse intrinsic antibiotic resistome from a cave bacterium. Nat Commun 2016;7:13803
167. Peirano G, Bradford PA, Kazmierczak KM et al. Global incidence of carbapenemase-producing Escherichia coli ST131. Emerg Infect Dis 2014;20:1928-31
168. Perichon B, Courvalin P. VanA-type vancomycin-resistant Staphylococcus aureus. Antimicrob Agents Ch 2009;53:4580-7
169. Pethe K, Sequeira PC, Agarwalla S et al. A chemical genetic screen in Mycobacterium tuberculosis identifies carbon-source-dependent growth inhibitors devoid of in vivo efficacy. Nat Commun 2010;1:57
170. Pettersson ME, Sun S, Andersson DI et al. Evolution of new gene functions: simulation and analysis of the amplification model. Genetica 2008;135:309-24
171. Phelan J, Coll F, McNerney R et al. Mycobacterium tuberculosis whole genome sequencing and protein structure modelling provides insights into anti-tuberculosis drug resistance. Bmc Med 2016;14:31
172. Pietsch F, Bergman JM, Brandis G et al. Ciprofloxacin selects for RNA polymerase mutations with pleiotropic antibiotic resistance effects. J Antimicrob Chemother 2017;72:75-84
173. Pitout JDD. Extraintestinal pathogenic Escherichia coli: a combination of virulence with antibiotic resistance. Front Microbiol 2012;3:9
174. Pittet LF, Posfay-Barbe KM. Pneumococcal vaccines for children: a global public health priority. Clin Microbiol Infect 2012;18 (Suppl 5):25-36
175. Prammananan T, Sander P, Brown BA et al. Single 16S ribosomal RNA substitution is responsible for resistance to amikacin and other 2-deoxystreptamine aminoglycosides in Mycobacterium abscessus and Mycobacterium chelonae. J Infect Dis 1998;177:1573-81
176. Price LB, Johnson JR, Aziz M et al. The epidemic of extendedspectrum-beta-lactamase-producing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. MBio 2013;4:e00377-313
177. Ramu H, Mankin A, Vazquez-Laslop N. Programmed drugdependent ribosome stalling. Mol Microbiol 2009;71:811-24
178. Reams AB, Kofoid E, SavageauMet al. Duplication frequency in a population of Salmonella enterica rapidly approaches steady state with or without recombination. Genetics 2010;184:1077-94
179. Roberts MC. Update on macrolide-lincosamide-streptogramin, ketolide, and oxazolidinone resistance genes. FEMS Microbiol Lett 2008;282:147-59
180. Rozen DE, McGee L, Levin BR et al. Fitness costs of fluoroquinolone resistance in Streptococcus pneumoniae. Antimicrob Agents Ch 2007;51:412-6
181. San Millan A, Heilbron K, MacLean RC. Positive epistasis between co-infecting plasmids promotes plasmid survival in bacterial populations. ISME J 2014;8:601-12
182. San Millan A, Pena-Miller R, Toll-Riera M et al. Positive selection and compensatory adaptation interact to stabilize nontransmissible plasmids. Nat Commun 2014;5:5208
183. Sato T, Yokota SI, Uchida I et al. Fluoroquinolone resistance mechanisms in an Escherichia coli isolate, HUE1, without quinolone resistance-determining region mutations. Front Microbiol 2013;4:125
184. Sauerbier J, Maurer P, Rieger M et al. Streptococcus pneumoniae R6 interspecies transformation: genetic analysis of penicillin resistance determinants and genome-wide recombination events. Mol Microbiol 2012;86:692-706
185. Schaible B, Taylor CT, Schaffer K. Hypoxia increases antibiotic resistance in Pseudomonas aeruginosa through altering the composition ofmultidrug efflux pumps. Antimicrob Agents Ch 2012;56:2114-8
186. Shcherbakov D, Akbergenov R, Matt T et al. Directed mutagenesis of Mycobacterium smegmatis 16S rRNA to reconstruct the in-vivo evolution of aminoglycoside resistance in Mycobacterium tuberculosis. Mol Microbiol 2010;77:830-40
187. Shih PC, Huang CT. Effects of quorum-sensing deficiency on Pseudomonas aeruginosa biofilm formation and antibiotic resistance. J Antimicrob Chemoth 2002;49:309-14
188. Sibold C, Henrichsen J, Konig A et al. Mosaic Pbpx genes of major clones of penicillin-resistant Streptococcus pneumoniae have evolved from Pbpx genes of a penicillin-sensitive Streptococcus oralis. Mol Microbiol 1994;12:1013-23
189. Silva RF, Mendonca SC, Carvalho LMet al. Pervasive sign epistasis between conjugative plasmids and drug-resistance chromosomal mutations. PLoS Genet 2011;7:e1002181
190. Sommer MO, Dantas G, Church GM. Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 2009;325:1128-31
191. Spratt BG, Hanage WP, Feil EJ. The relative contributions of recombination and point mutation to the diversification of bacterial clones. Curr Opin Microbiol 2001;4:602-6
192. Srivatsan A, Wang JD. Control of bacterial transcription, translation and replication by (p)ppGpp. Curr Opin Microbiol 2008;11:100-5
193. StenstromTA, Conway P, Kjelleberg S. Inhibition by antibiotics of the bacterial response to long-term starvation of Salmonella Typhimurium and the colon microbiota of mice. J Appl Bacteriol 1989;67:53-9
194. Stoesser N, Sheppard AE, Pankhurst L et al. Evolutionary history of the global emergence of the Escherichia coli epidemic clone ST131. MBio 2016;7:e02162
195. Stoesser N, Sheppard AE, Peirano G et al. First report of blaIMP-14 on a plasmid harboring multiple drug resistance genes in Escherichia coli sequence type 131. Antimicrob Agents Ch 2016;60:5068-71
196. Strahilevitz J, Jacoby GA, Hooper DC et al. Plasmid-mediated quinolone resistance: amultifaceted threat. Clin Microbiol Rev 2009;22:664-89
197. Straume D, Stamsas GA, Havarstein LS. Natural transformation and genome evolution in Streptococcus pneumoniae. Infect Genet Evol 2015;33:371-80
198. Sutherland R, Rolinson GN. Characteristics of methicillinresistant staphylococci. J Bacteriol 1964;87:887-99
199. Tan C, Smith RP, Srimani JK et al. The inoculum effect and bandpass bacterial response to periodic antibiotic treatment. Mol Syst Biol 2012;8:617
200. Tapsall JW. Neisseria gonorrhoeae and emerging resistance to extended spectrum cephalosporins. Curr Opin Infect Dis 2009;22:87-91
201. Taylor PK, Yeung AT, Hancock RE. Antibiotic resistance in Pseudomonas aeruginosa biofilms: towards the development of novel anti-biofilm therapies. J Biotechnol 2014;191:121-30
202. Tettelin H, Masignani V, Cieslewicz MJ et al. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial 'pan-genome'. P Natl Acad Sci USA 2005;102:13950-5
203. Thulin E, Sundqvist M, Andersson DI. Amdinocillin (mecillinam) resistance mutations in clinical isolates and laboratoryselected mutants of Escherichia coli. Antimicrob Agents Ch 2015;59:1723-32
204. Torres A, Bonanni P, HryniewiczWet al. Pneumococcal vaccination: what have we learnt so far and what can we expect in the future? Eur J Clin Microbiol 2015;34:19-31
205. Tran JH, Jacoby GA. Mechanism of plasmid-mediated quinolone resistance. P Natl Acad Sci USA 2002;99:5638-42
206. Trindade S, Sousa A, Xavier KB et al. Positive epistasis drives the acquisition of multidrug resistance. PLoS Genet 2009;5:e1000578
207. Tuomanen E, Cozens R, Tosch W et al. The rate of killing of Escherichia coli by beta-lactam antibiotics is strictly proportional to the rate of bacterial growth. J Gen Microbiol 1986;132:1297-304
208. Vazquez-Laslop N, Thum C, Mankin AS. Molecular mechanism of drug-dependent ribosome stalling. Mol Cell 2008;30:190-202
209. Villa J, Viedma E, Branas P et al. Draft whole-genome sequence of OXA-48-producing multidrug-resistant Klebsiella pneumoniae KP ST11 OXA-48. Genome Announc 2014;2:e00737-00714
210. Villa L, Capone A, Fortini D et al. Reversion to susceptibility of a carbapenem-resistant clinical isolate of Klebsiella pneumoniae producing KPC-3. J Antimicrob Chemoth 2013;68:2482-6
211. Vincent JL. Nosocomial infections in adult intensive-care units. Lancet 2003;361:2068-77
212. Vogwill T, MacLean RC. The genetic basis of the fitness costs of antimicrobial resistance: a meta-analysis approach. Evol Appl 2015;8:284-95
213. Vogwill T, Kojadinovic M, MacLean RC. Epistasis between antibiotic resistancemutations and genetic background shape the fitness effect of resistance across species of Pseudomonas. Proc Biol Sci 2016;283:20160151
214. Voulgari E, Gartzonika C, Vrioni G et al. The Balkan region: NDM-1-producing Klebsiella pneumoniae ST11 clonal strain causing outbreaks in Greece. J Antimicrob Chemother 2014; 69:2091-7
215. Walters MC, Roe F, Bugnicourt A et al. Contributions of antibiotic penetration, oxygen limitation, and low metabolic activity to tolerance of Pseudomonas aeruginosa biofilms to ciprofloxacin and tobramycin. Antimicrob Agents Ch 2003;47:317-23
216. Walther-Rasmussen J, Hoiby N. Class A carbapenemases. J Antimicrob Chemoth 2007;60:470-82
217. Wang H, Dzink-Fox JL, Chen M et al. Genetic characterization of highly fluoroquinolone-resistant clinical Escherichia coli strains from China: role of acrR mutations. Antimicrob Agents Ch 2001;45:1515-21
218. Ward H, Perron GG, Maclean RC. The cost of multiple drug resistance in Pseudomonas aeruginosa. J Evol Biol 2009;22:997-1003
219. WebberM, Piddock LJV. Quinolone resistance in Escherichia coli. Vet Res 2001;32:275-84
220. Whitney CG, Farley MM, Hadler J et al. Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine. New Engl J Med 2003;348:1737-46
221. WHO. Antimicrobial Resistance: Global Report On Surveillance 2014. 2014, Geneva, Switzerland: World Health Organization
222. Winstanley C, O'Brien S, Brockhurst MA. Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol 2016;24:327-37
223. Woodford N, Carattoli A, Karisik E et al. Complete nucleotide sequences of plasmids pEK204, pEK499, and pEK516, encoding CTX-M enzymes in three major Escherichia coli lineages from the United Kingdom, all belonging to the international O25:H4-ST131 clone. Antimicrob Agents Ch 2009; 53:4472-82
224. Wu J, Long QX, Xie JP. (p)ppGpp and drug resistance. J Cell Physiol 2010;224:300-4
225. Yeung AT, Bains M, Hancock RE. The sensor kinase CbrA is a global regulator that modulates metabolism, virulence, and antibiotic resistance in Pseudomonas aeruginosa. J Bacteriol 2011;193:918-31
226. Yurtsev EA, Chao HX, Datta MS et al. Bacterial cheating drives the population dynamics of cooperative antibiotic resistance plasmids. Mol Syst Biol 2013;9:683
227. Zhang L, Hinz AJ, Nadeau JP et al. Pseudomonas aeruginosa tssC1 links type VI secretion and biofilm-specific antibiotic resistance. J Bacteriol 2011;193:5510-3