1932

Abstract

By targeting essential cellular processes, antibiotics provoke metabolic perturbations and induce stress responses and genetic variation in bacteria. Here we review current knowledge of the mechanisms by which these molecules generate genetic instability. They include production of reactive oxygen species, as well as induction of the stress response regulons, which lead to enhancement of mutation and recombination rates and modulation of horizontal gene transfer. All these phenomena influence the evolution and spread of antibiotic resistance. The use of strategies to stop or decrease the generation of resistant variants is also discussed.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-090817-062139
2018-09-08
2024-04-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/72/1/annurev-micro-090817-062139.html?itemId=/content/journals/10.1146/annurev-micro-090817-062139&mimeType=html&fmt=ahah

Literature Cited

  1. 1.  Aarestrup FM 2005. Veterinary drug usage and antimicrobial resistance in bacteria of animal origin. Basic Clin. Pharmacol. Toxicol. 96:271–81
    [Google Scholar]
  2. 2.  Al Mamun AA, Gautam S, Humayun MZ 2006. Hypermutagenesis in mutA cells is mediated by mistranslational corruption of polymerase, and is accompanied by replication fork collapse. Mol. Microbiol. 62:1752–63
    [Google Scholar]
  3. 3.  Alam MK, Alhhazmi A, DeCoteau JF, Luo Y, Geyer CR 2016. RecA inhibitors potentiate antibiotic activity and block evolution of antibiotic resistance. Cell Chem. Biol. 23:381–91
    [Google Scholar]
  4. 4.  Amabile-Cuevas CF, Heinemann JA 2004. Shooting the messenger of antibiotic resistance: plasmid elimination as a potential counter-evolutionary tactic. Drug Discov. Today 9:465–67
    [Google Scholar]
  5. 5.  Andersson DI, Hughes D 2014. Microbiological effects of sublethal levels of antibiotics. Nat. Rev. Microbiol. 12:465–78
    [Google Scholar]
  6. 6.  Appelbaum PC 2012. 2012 and beyond: potential for the start of a second pre-antibiotic era?. J. Antimicrob. Chemother. 67:2062–68
    [Google Scholar]
  7. 7.  Aranda J, Lopez M, Leiva E, Magan A, Adler B et al. 2014. Role of Acinetobacter baumannii UmuD homologs in antibiotic resistance acquired through DNA damage-induced mutagenesis. Antimicrob. Agents Chemother. 58:1771–73
    [Google Scholar]
  8. 8.  Arriaga-Alba M, Rivera-Sanchez R, Parra-Cervantes G, Barro-Moreno F, Flores-Paz R, Garcia-Jimenez E 2000. Antimutagenesis of β-carotene to mutations induced by quinolone on Salmonella typhimurium. Arch. Med. Res. 31:156–61
    [Google Scholar]
  9. 9.  Baharoglu Z, Babosan A, Mazel D 2014. Identification of genes involved in low aminoglycoside-induced SOS response in Vibrio cholerae: a role for transcription stalling and Mfd helicase. Nucleic Acids Res 42:2366–79
    [Google Scholar]
  10. 10.  Baharoglu Z, Krin E, Mazel D 2013. RpoS plays a central role in the SOS induction by sub-lethal aminoglycoside concentrations in Vibrio cholerae. . PLOS Genet 9:4e1003421 https://doi.org/10.1371/journal.pgen.1003421
    [Crossref] [Google Scholar]
  11. 11.  Baharoglu Z, Mazel D 2011. Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance. Antimicrob. Agents Chemother. 55:2438–41
    [Google Scholar]
  12. 12.  Baquero F 2001. Low-level antibacterial resistance: a gateway to clinical resistance. Drug Resist. Updates 4:93–105
    [Google Scholar]
  13. 13.  Baquero F, Coque TM, de la Cruz F 2011. Ecology and evolution as targets: the need for novel eco-evo drugs and strategies to fight antibiotic resistance. Antimicrob. Agents Chemother. 55:3649–60
    [Google Scholar]
  14. 14.  Baquero F, Lanza VF, Canton R, Coque TM 2015. Public health evolutionary biology of antimicrobial resistance: priorities for intervention. Evol. Appl. 8:223–39
    [Google Scholar]
  15. 15.  Baquero F, Negri MC 1997. Selective compartments for resistant microorganisms in antibiotic gradients. BioEssays 19:731–36
    [Google Scholar]
  16. 16.  Barbe J, Villaverde A, Guerrero R 1983. Evolution of cellular ATP concentration after UV-mediated induction of SOS system in Escherichia coli. Biochem. Biophys. Res. Commun. 117:556–61
    [Google Scholar]
  17. 17.  Battesti A, Majdalani N, Gottesman S 2011. The RpoS-mediated general stress response in Escherichia coli. Annu. Rev. Microbiol. 65:189–213
    [Google Scholar]
  18. 18.  Belenky P, Ye JD, Porter CB, Cohen NR, Lobritz MA et al. 2015. Bactericidal antibiotics induce toxic metabolic perturbations that lead to cellular damage. Cell Rep 13:968–80
    [Google Scholar]
  19. 19.  Bellio P, Brisdelli F, Perilli M, Sabatini A, Bottoni C et al. 2014. Curcumin inhibits the SOS response induced by levofloxacin in Escherichia coli. . Phytomedicine 21:430–34
    [Google Scholar]
  20. 20.  Bellio P, Di Pietro L, Mancini A, Piovano M, Nicoletti M et al. 2017. SOS response in bacteria: inhibitory activity of lichen secondary metabolites against Escherichia coli RecA protein. Phytomedicine 29:11–18
    [Google Scholar]
  21. 21.  Bernier SP, Lebeaux D, DeFrancesco AS, Valomon A, Soubigou G et al. 2013. Starvation, together with the SOS response, mediates high biofilm-specific tolerance to the fluoroquinolone ofloxacin. PLOS Genet 9:e1003144
    [Google Scholar]
  22. 22.  Blázquez J 2003. Hypermutation as a factor contributing to the acquisition of antimicrobial resistance. Clin. Infect. Dis. 37:1201–9
    [Google Scholar]
  23. 23.  Boshoff HI, Reed MB, Barry CE 3rd, Mizrahi V 2003. DnaE2 polymerase contributes to in vivo survival and the emergence of drug resistance in Mycobacterium tuberculosis. . Cell 113:183–93
    [Google Scholar]
  24. 24.  Bunnell BE, Escobar JF, Bair KL, Sutton MD, Crane JK 2017. Zinc blocks SOS-induced antibiotic resistance via inhibition of RecA in Escherichia coli. . PLOS ONE 12:e0178303
    [Google Scholar]
  25. 25.  Cabello FC 2006. Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ. Microbiol. 8:1137–44
    [Google Scholar]
  26. 26.  Cabezon E, de la, Cruz F, Arechaga I 2017. Conjugation inhibitors and their potential use to prevent dissemination of antibiotic resistance genes in bacteria. Front. Microbiol. 8:2329
    [Google Scholar]
  27. 27.  Castaneda-Garcia A, Prieto AI, Rodriguez-Beltran J, Alonso N, Cantillon D et al. 2017. A non-canonical mismatch repair pathway in prokaryotes. Nat. Commun. 8:14246
    [Google Scholar]
  28. 28.  Chiang SM, Schellhorn HE 2010. Evolution of the RpoS regulon: origin of RpoS and the conservation of RpoS-dependent regulation in bacteria. J. Mol. Evol. 70:557–71
    [Google Scholar]
  29. 29.  Ciofu O, Mandsberg LF, Bjarnsholt T, Wassermann T, Hoiby N 2010. Genetic adaptation of Pseudomonas aeruginosa during chronic lung infection of patients with cystic fibrosis: strong and weak mutators with heterogeneous genetic backgrounds emerge in mucA and/or lasR mutants. Microbiology 156:1108–19
    [Google Scholar]
  30. 30.  Cirz RT, Chin JK, Andes DR, de Crecy-Lagard V, Craig WA, Romesberg FE 2005. Inhibition of mutation and combating the evolution of antibiotic resistance. PLOS Biol 3:e176
    [Google Scholar]
  31. 31.  Cirz RT, Romesberg FE 2007. Controlling mutation: intervening in evolution as a therapeutic strategy. Crit. Rev. Biochem. Mol. Biol. 42:341–54
    [Google Scholar]
  32. 32.  Cline DJ, Holt SL, Singleton SF 2007. Inhibition of Escherichia coli RecA by rationally redesigned N-terminal helix. Org. Biomol. Chem. 5:1525–28
    [Google Scholar]
  33. 33.  Couce A, Blázquez J 2009. Side effects of antibiotics on genetic variability. FEMS Microbiol. Rev. 33:531–38
    [Google Scholar]
  34. 34.  Cox EC, Gibson TC 1974. Selection for high mutation rates in chemostats. Genetics 77:169–84
    [Google Scholar]
  35. 35.  Cox MM 2007. Regulation of bacterial RecA protein function. Crit. Rev. Biochem. Mol. Biol. 42:41–63
    [Google Scholar]
  36. 36.  Crane JK, Broome JE, Reddinger RM, Werth BB 2014. Zinc protects against Shiga-toxigenic Escherichia coli by acting on host tissues as well as on bacteria. BMC Microbiol 14:145
    [Google Scholar]
  37. 37.  Culyba MJ, Mo CY, Kohli RM 2015. Targets for combating the evolution of acquired antibiotic resistance. Biochemistry 54:3573–82
    [Google Scholar]
  38. 38.  Dahan-Grobgeld E, Livneh Z, Maretzek AF, Polak-Charcon S, Eichenbaum Z, Degani H 1998. Reversible induction of ATP synthesis by DNA damage and repair in Escherichia coli: in vivo NMR studies. J. Biol. Chem. 273:30232–38
    [Google Scholar]
  39. 39.  Dapa T, Fleurier S, Bredeche MF, Matic I 2017. The SOS and RpoS regulons contribute to bacterial cell robustness to genotoxic stress by synergistically regulating DNA polymerase pol II. Genetics 206:1349–60
    [Google Scholar]
  40. 40.  Davies J 1994. Inactivation of antibiotics and the dissemination of resistance genes. Science 264:375–82
    [Google Scholar]
  41. 41.  Davies J, Spiegelman GB, Yim G 2006. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 9:445–53
    [Google Scholar]
  42. 42.  Denamur E, Matic I 2006. Evolution of mutation rates in bacteria. Mol. Microbiol. 60:820–27
    [Google Scholar]
  43. 43.  Denamur E, Tenaillon O, Deschamps C, Skurnik D, Ronco E et al. 2005. Intermediate mutation frequencies favor evolution of multidrug resistance in Escherichia coli. . Genetics 171:825–27
    [Google Scholar]
  44. 44.  Didelot X, Maiden MC 2010. Impact of recombination on bacterial evolution. Trends Microbiol 18:315–22
    [Google Scholar]
  45. 45.  Didier JP, Villet R, Huggler E, Lew DP, Hooper DC et al. 2011. Impact of ciprofloxacin exposure on Staphylococcus aureus genomic alterations linked with emergence of rifampin resistance. Antimicrob. Agents Chemother. 55:1946–52
    [Google Scholar]
  46. 46.  Dorr T, Lewis K, Vulic M 2009. SOS response induces persistence to fluoroquinolones in Escherichia coli. . PLOS Genet 5:e1000760
    [Google Scholar]
  47. 47.  Dwyer DJ, Belenky PA, Yang JH, MacDonald IC, Martell JD et al. 2014. Antibiotics induce redox-related physiological alterations as part of their lethality. PNAS 111:E2100–9
    [Google Scholar]
  48. 48.  Erill I, Campoy S, Barbe J 2007. Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol. Rev. 31:637–56
    [Google Scholar]
  49. 49.  Fornelos N, Browning DF, Butala M 2016. The use and abuse of LexA by mobile genetic elements. Trends Microbiol 24:391–401
    [Google Scholar]
  50. 50.  Foster PL 2007. Stress-induced mutagenesis in bacteria. Crit. Rev. Biochem. Mol. Biol. 42:373–97
    [Google Scholar]
  51. 51.  Foti JJ, Devadoss B, Winkler JA, Collins JJ, Walker GC 2012. Oxidation of the guanine nucleotide pool underlies cell death by bactericidal antibiotics. Science 336:315–19
    [Google Scholar]
  52. 52.  Frenoy A, Bonhoeffer S 2018. Death and population dynamics affect mutation rate estimates and evolvability under stress in bacteria. PLOS Biol 16:5e2005056
    [Google Scholar]
  53. 53.  Frisch RL, Su Y, Thornton PC, Gibson JL, Rosenberg SM, Hastings PJ 2010. Separate DNA Pol II- and Pol IV-dependent pathways of stress-induced mutation during double-strand-break repair in Escherichia coli are controlled by RpoS. J. Bacteriol. 192:4694–700
    [Google Scholar]
  54. 54.  Fung-Tomc J, Kolek B, Bonner DP 1993. Ciprofloxacin-induced, low-level resistance to structurally unrelated antibiotics in Pseudomonas aeruginosa and methicillin-resistant Staphylococcus aureus. Antimicrob. . Agents Chemother 37:1289–96
    [Google Scholar]
  55. 55.  Gibson TC, Scheppe ML, Cox EC 1970. Fitness of an Escherichia coli mutator gene. Science 169:686–88
    [Google Scholar]
  56. 56.  Gillespie SH, Basu S, Dickens AL, O'Sullivan DM, McHugh TD 2005. Effect of subinhibitory concentrations of ciprofloxacin on Mycobacterium fortuitum mutation rates. J. Antimicrob. Chemother. 56:344–48
    [Google Scholar]
  57. 57.  Giroux X, Su W, Bredeche M, Matic I 2017. Maladaptive DNA repair activity is the ultimate contributor to the death of trimethoprim-treated cells under aerobic and anaerobic conditions. PNAS 114:11512–17
    [Google Scholar]
  58. 58.  Goerke C, Koller J, Wolz C 2006. Ciprofloxacin and trimethoprim cause phage induction and virulence modulation in Staphylococcus aureus. Antimicrob. Agents Chemother 50:171–77
    [Google Scholar]
  59. 59.  Goh EB, Yim G, Tsui W, McClure J, Surette MG, Davies J 2002. Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. PNAS 99:17025–30
    [Google Scholar]
  60. 60.  Goneau LW, Hannan TJ, MacPhee RA, Schwartz DJ, Macklaim JM et al. 2015. Subinhibitory antibiotic therapy alters recurrent urinary tract infection pathogenesis through modulation of bacterial virulence and host immunity. mBio 6:e00356–15
    [Google Scholar]
  61. 61.  Goodman MF 2014. The discovery of error-prone DNA polymerase V and its unique regulation by RecA and ATP. J. Biol. Chem. 289:26772–82
    [Google Scholar]
  62. 62.  Goswami M, Mangoli SH, Jawali N 2006. Involvement of reactive oxygen species in the action of ciprofloxacin against Escherichia coli. Antimicrob. Agents Chemother 50:949–54
    [Google Scholar]
  63. 63.  Goulas A, Haudin CS, Bergheaud V, Dumeny V, Ferhi S et al. 2016. A new extraction method to assess the environmental availability of ciprofloxacin in agricultural soils amended with exogenous organic matter. Chemosphere 165:460–69
    [Google Scholar]
  64. 64.  Guerin E, Cambray G, Sanchez-Alberola N, Campoy S, Erill I et al. 2009. The SOS response controls integron recombination. Science 324:1034
    [Google Scholar]
  65. 65.  Gullberg E, Cao S, Berg OG, Ilback C, Sandegren L et al. 2011. Selection of resistant bacteria at very low antibiotic concentrations. PLOS Pathog 7:e1002158
    [Google Scholar]
  66. 66.  Gutierrez A, Laureti L, Crussard S, Abida H, Rodríguez-Rojas A et al. 2013. β-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediated reduction in replication fidelity. Nat. Commun. 4:1610
    [Google Scholar]
  67. 67.  Hastings PJ, Rosenberg SM, Slack A 2004. Antibiotic-induced lateral transfer of antibiotic resistance. Trends Microbiol 12:401–4
    [Google Scholar]
  68. 68.  Henderson-Begg SK, Livermore DM, Hall LM 2006. Effect of subinhibitory concentrations of antibiotics on mutation frequency in Streptococcus pneumoniae. J. Antimicrob. Chemother. 57:849–54
    [Google Scholar]
  69. 69.  Hisama M, Matsuda S, Shibayama H, Iwaki M 2008. Antimutagenic activity of a novel ascorbic derivative, disodium isostearyl 2-O-l-ascorbyl phosphate. Yakugaku Zasshi 128:933–40
    [Google Scholar]
  70. 70.  Hisama M, Matsuda S, Tanaka T, Shibayama H, Nomura M, Iwaki M 2008. Suppression of mutagens-induced SOS response by phytoncide solution using Salmonella typhimurium TA1535/pSK1002 umu test. J. Oleo Sci. 57:381–90
    [Google Scholar]
  71. 71.  Hocquet D, Bertrand X 2014. Metronidazole increases the emergence of ciprofloxacin- and amikacin-resistant Pseudomonas aeruginosa by inducing the SOS response. J. Antimicrob. Chemother. 69:852–54
    [Google Scholar]
  72. 72.  Hocquet D, Llanes C, Thouverez M, Kulasekara HD, Bertrand X et al. 2012. Evidence for induction of integron-based antibiotic resistance by the SOS response in a clinical setting. PLOS Pathog 8:e1002778
    [Google Scholar]
  73. 73.  Holmes AH, Moore LS, Sundsfjord A, Steinbakk M, Regmi S et al. 2016. Understanding the mechanisms and drivers of antimicrobial resistance. Lancet 387:176–87
    [Google Scholar]
  74. 74.  Huerta-Uribe A, Marjenberg ZR, Yamaguchi N, Fitzgerald S, Connolly JP et al. 2016. Identification and characterization of novel compounds blocking Shiga toxin expression in Escherichia coli O157:H7. Front. Microbiol. 7:1930
    [Google Scholar]
  75. 75.  Hughes D, Andersson DI 2012. Selection of resistance at lethal and non-lethal antibiotic concentrations. Curr. Opin. Microbiol. 15:555–60
    [Google Scholar]
  76. 76.  Hughes D, Andersson DI 2017. Evolutionary trajectories to antibiotic resistance. Annu. Rev. Microbiol. 71:579–96
    [Google Scholar]
  77. 77.  Imamovic L, Sommer MO 2013. Use of collateral sensitivity networks to design drug cycling protocols that avoid resistance development. Sci. Transl. Med. 5:204ra132
    [Google Scholar]
  78. 78.  Imlay JA 2009. Oxidative stress. EcoSal Plus 2009. https://doi.org/10.1128/ecosalplus.5.4.4
    [Crossref] [Google Scholar]
  79. 79.  Ippoliti PJ, Delateur NA, Jones KM, Beuning PJ 2012. Multiple strategies for translesion synthesis in bacteria. Cells 1:799–831
    [Google Scholar]
  80. 80.  Jara LM, Perez-Varela M, Corral J, Arch M, Cortes P et al. 2015. Novobiocin inhibits the antimicrobial resistance acquired through DNA damage-induced mutagenesis in Acinetobacter baumannii. Antimicrob. Agents Chemother 60:637–39
    [Google Scholar]
  81. 81.  Jee J, Rasouly A, Shamovsky I, Akivis Y, Steinman SR et al. 2016. Rates and mechanisms of bacterial mutagenesis from maximum-depth sequencing. Nature 534:693–96
    [Google Scholar]
  82. 82.  Jones-Lepp TL 2006. Chemical markers of human waste contamination: analysis of urobilin and pharmaceuticals in source waters. J. Environ. Monit. 8:472–78
    [Google Scholar]
  83. 83.  Kamruzzaman M, Shoma S, Thomas CM, Partridge SR, Iredell JR 2017. Plasmid interference for curing antibiotic resistance plasmids in vivo. PLOS ONE 12:e0172913
    [Google Scholar]
  84. 84.  Kasprzyk-Hordern B, Dinsdale RM, Guwy AJ 2008. The occurrence of pharmaceuticals, personal care products, endocrine disruptors and illicit drugs in surface water in South Wales, UK. Water Res 42:3498–518
    [Google Scholar]
  85. 85.  Kim S, Lieberman TD, Kishony R 2014. Alternating antibiotic treatments constrain evolutionary paths to multidrug resistance. PNAS 111:14494–99
    [Google Scholar]
  86. 86.  Kohanski MA, DePristo MA, Collins JJ 2010. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 37:311–20
    [Google Scholar]
  87. 87.  Konola JT, Sargent KE, Gow JB 2000. Efficient repair of hydrogen peroxide-induced DNA damage by Escherichia coli requires SOS induction of RecA and RuvA proteins. Mutat. Res. 459:187–94
    [Google Scholar]
  88. 88.  Laureti L, Matic I, Gutierrez A 2013. Bacterial responses and genome instability induced by subinhibitory concentrations of antibiotics. Antibiotics 2:100–14
    [Google Scholar]
  89. 89.  Lee AM, Ross CT, Zeng BB, Singleton SF 2005. A molecular target for suppression of the evolution of antibiotic resistance: inhibition of the Escherichia coli RecA protein by N6-(1-naphthyl)-ADP. J. Med. Chem. 48:5408–11
    [Google Scholar]
  90. 90.  Lee AM, Singleton SF 2004. Inhibition of the Escherichia coli RecA protein: zinc(II), copper(II) and mercury(II) trap RecA as inactive aggregates. J. Inorg. Biochem. 98:1981–86
    [Google Scholar]
  91. 91.  Letchumanan V, Chan KG, Lee LH 2015. An insight of traditional plasmid curing in Vibrio species. Front. Microbiol. 6:735
    [Google Scholar]
  92. 92.  Levin DE, Marnett LJ, Ames BN 1984. Spontaneous and mutagen-induced deletions: mechanistic studies in Salmonella tester strain TA102. PNAS 81:4457–61
    [Google Scholar]
  93. 93.  Lewin CS, Amyes SG 1991. The role of the SOS response in bacteria exposed to zidovudine or trimethoprim. J. Med. Microbiol. 34:329–32
    [Google Scholar]
  94. 94.  Liu P, Wu Z, Xue H, Zhao X 2017. Antibiotics trigger initiation of SCCmec transfer by inducing SOS responses. Nucleic Acids Res 45:3944–52
    [Google Scholar]
  95. 95.  Lobritz MA, Belenky P, Porter CB, Gutierrez A, Yang JH et al. 2015. Antibiotic efficacy is linked to bacterial cellular respiration. PNAS 112:8173–80
    [Google Scholar]
  96. 96.  Long H, Miller SF, Strauss C, Zhao C, Cheng L et al. 2016. Antibiotic treatment enhances the genome-wide mutation rate of target cells. PNAS 113:E2498–505
    [Google Scholar]
  97. 97.  López E, Elez M, Matic I, Blázquez J 2007. Antibiotic-mediated recombination: ciprofloxacin stimulates SOS-independent recombination of divergent sequences in Escherichia coli. Mol. Microbiol. 64:83–93
    [Google Scholar]
  98. 98.  Lorian V 1975. Some effects of subinhibitory concentrations of antibiotics on bacteria. Bull. N. Y. Acad. Med. 51:1046–55
    [Google Scholar]
  99. 99.  Lu TK, Collins JJ 2009. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. PNAS 106:4629–34
    [Google Scholar]
  100. 100.  Maciá MD, Blanquer D, Togores B, Sauleda J, Pérez JL, Oliver A 2005. Hypermutation is a key factor in development of multiple-antimicrobial resistance in Pseudomonas aeruginosa strains causing chronic lung infections. Antimicrob. Agents Chemother. 49:3382–86
    [Google Scholar]
  101. 101.  Maiques E, Ubeda C, Campoy S, Salvador N, Lasa I et al. 2006. β-Lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J. Bacteriol. 188:2726–29
    [Google Scholar]
  102. 102.  Mao EF, Lane L, Lee J, Miller JH 1997. Proliferation of mutators in A cell population. J. Bacteriol. 179:417–22
    [Google Scholar]
  103. 103.  Mathieu A, Fleurier S, Frenoy A, Dairou J, Bredeche MF et al. 2016. Discovery and function of a general core hormetic stress response in E. coli induced by sublethal concentrations of antibiotics. Cell Rep 17:46–57
    [Google Scholar]
  104. 104.  McManus PS, Stockwell VO, Sundin GW, Jones AL 2002. Antibiotic use in plant agriculture. Annu. Rev. Phytopathol. 40:443–65
    [Google Scholar]
  105. 105.  Miller C, Thomsen LE, Gaggero C, Mosseri R, Ingmer H, Cohen SN 2004. SOS response induction by β-lactams and bacterial defense against antibiotic lethality. Science 305:1629–31
    [Google Scholar]
  106. 106.  Miller JH 1998. Mutators in Escherichia coli. Mutat. Res. 409:99–106
    [Google Scholar]
  107. 107.  Miyazawa M, Hisama M 2003. Antimutagenic activity of flavonoids from Chrysanthemum morifolium. Biosci. Biotechnol. Biochem. 67:2091–99
    [Google Scholar]
  108. 108.  Miyazawa M, Sakano K, Nakamura S, Kosaka H 1999. Antimutagenic activity of isoflavones from soybean seeds (Glycine max Merrill). J. Agric. Food Chem. 47:1346–49
    [Google Scholar]
  109. 109.  Miyazawa M, Sakano K, Nakamura S, Kosaka H 2001. Antimutagenic activity of isoflavone from Pueraria lobata. J. Agric. Food Chem. 49:336–41
    [Google Scholar]
  110. 110.  Mo CY, Culyba MJ, Selwood T, Kubiak JM, Hostetler ZM et al. 2018. Inhibitors of LexA autoproteolysis and the bacterial SOS response discovered by an academic-industry partnership. ACS Infect. Dis. 4:349–59
    [Google Scholar]
  111. 111.  Mo CY, Manning SA, Roggiani M, Culyba MJ, Samuels AN et al. 2016. Systematically altering bacterial SOS activity under stress reveals therapeutic strategies for potentiating antibiotics. mSphere 1:e00163–16
    [Google Scholar]
  112. 112.  Nagel M, Reuter T, Jansen A, Szekat C, Bierbaum G 2011. Influence of ciprofloxacin and vancomycin on mutation rate and transposition of IS256 in Staphylococcus aureus. Int. J. Med. Microbiol. 301:229–36
    [Google Scholar]
  113. 113.  Nair CG, Chao C, Ryall B, Williams HD 2012. Sub‐lethal concentrations of antibiotics increase mutation frequency in the cystic fibrosis pathogen Pseudomonas aeruginosa. Lett. Appl. Microbiol. 56:149–54
    [Google Scholar]
  114. 114.  Nautiyal A, Patil KN, Muniyappa K 2014. Suramin is a potent and selective inhibitor of Mycobacterium tuberculosis RecA protein and the SOS response: RecA as a potential target for antibacterial drug discovery. J. Antimicrob. Chemother. 69:1834–43
    [Google Scholar]
  115. 115.  Newcombe HB 1949. Origin of bacterial variants. Nature 164:150
    [Google Scholar]
  116. 116.  Nohmi T 2006. Environmental stress and lesion-bypass DNA polymerases. Annu. Rev. Microbiol. 60:231–53
    [Google Scholar]
  117. 117.  Oethinger M, Kern WV, Jellen-Ritter AS, McMurry LM, Levy SB 2000. Ineffectiveness of topoisomerase mutations in mediating clinically significant fluoroquinolone resistance in Escherichia coli in the absence of the AcrAB efflux pump. Antimicrob. Agents Chemother. 44:10–13
    [Google Scholar]
  118. 118.  Ojala V, Laitalainen J, Jalasvuori M 2013. Fight evolution with evolution: plasmid-dependent phages with a wide host range prevent the spread of antibiotic resistance. Evol. Appl. 6:925–32
    [Google Scholar]
  119. 119.  Oliver A, Baquero F, Blázquez J 2002. The mismatch repair system (mutS, mutL and uvrD genes) in Pseudomonas aeruginosa: molecular characterization of naturally occurring mutants. Mol. Microbiol. 43:1641–50
    [Google Scholar]
  120. 120.  Oliver A, Cantón R, Campo P, Baquero F, Blázquez J 2000. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288:1251–54
    [Google Scholar]
  121. 121.  Orlen H, Hughes D 2006. Weak mutators can drive the evolution of fluoroquinolone resistance in Escherichia coli. Antimicrob. Agents Chemother. 50:3454–56
    [Google Scholar]
  122. 122.  Pal C, Papp B, Lazar V 2015. Collateral sensitivity of antibiotic-resistant microbes. Trends Microbiol 23:401–7
    [Google Scholar]
  123. 123.  Peng Q, Zhou S, Yao F, Hou B, Huang Y et al. 2011. Baicalein suppresses the SOS response system of Staphylococcus aureus induced by ciprofloxacin. Cell Physiol. Biochem. 28:1045–50
    [Google Scholar]
  124. 124.  Pérez-Capilla T, Baquero MR, Gómez-Gómez JM, Ionel A, Martín S, Blázquez J 2005. SOS-independent induction of dinB transcription by β-lactam-mediated inhibition of cell wall synthesis in Escherichia coli. J. Bacteriol. 187:1515–18
    [Google Scholar]
  125. 125.  Peterson EJ, Janzen WP, Kireev D, Singleton SF 2012. High-throughput screening for RecA inhibitors using a transcreener adenosine 5′-O-diphosphate assay. Assay Drug Dev. Technol. 10:260–68
    [Google Scholar]
  126. 126.  Phillips I, Culebras E, Moreno F, Baquero F 1987. Induction of the SOS response by new 4-quinolones. J. Antimicrob. Chemother. 20:631–38
    [Google Scholar]
  127. 127.  Pietta PG 2000. Flavonoids as antioxidants. J. Nat. Prod. 63:1035–42
    [Google Scholar]
  128. 128.  Pletz MW, Rau M, Bulitta J, De Roux A, Burkhardt O et al. 2004. Ertapenem pharmacokinetics and impact on intestinal microflora, in comparison to those of ceftriaxone, after multiple dosing in male and female volunteers. Antimicrob. Agents Chemother. 48:3765–72
    [Google Scholar]
  129. 129.  Pomerantz RT, Goodman MF, O'Donnell ME 2013. DNA polymerases are error-prone at RecA-mediated recombination intermediates. Cell Cycle 12:2558–63
    [Google Scholar]
  130. 130.  Quoc Tuc D, Elodie MG, Pierre L, Fabrice A, Marie-Jeanne T et al. 2017. Fate of antibiotics from hospital and domestic sources in a sewage network. Sci. Total Environ. 575:758–66
    [Google Scholar]
  131. 131.  Radman M, Taddei F, Matic I 2000. Evolution-driving genes. Res. Microbiol. 151:91–95
    [Google Scholar]
  132. 132.  Rayssiguier C, Thaler DS, Radman M 1989. The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342:396–401
    [Google Scholar]
  133. 133.  Recacha E, Machuca J, Diaz de Alba P, Ramos-Guelfo M, Docobo-Perez F et al. 2017. Quinolone resistance reversion by targeting the SOS response. mBio 8:e00971–17
    [Google Scholar]
  134. 134.  Ren L, Rahman MS, Humayun MZ 1999. Escherichia coli cells exposed to streptomycin display a mutator phenotype. J. Bacteriol. 181:1043–44
    [Google Scholar]
  135. 135.  Rodríguez-Beltrán J, Tourret J, Tenaillon O, López E, Bourdelier E et al. 2015. High recombinant frequency in extraintestinal pathogenic Escherichia coli strains. Mol. Biol. Evol. 32:1708–16
    [Google Scholar]
  136. 136.  Rodríguez-Rojas A, Couce A, Blázquez J 2010. Frequency of spontaneous resistance to fosfomycin combined with different antibiotics in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 54:4948–49
    [Google Scholar]
  137. 137.  Rodríguez-Rojas A, Makarova O, Rolff J 2014. Antimicrobials, stress and mutagenesis. PLOS Pathog 10:e1004445
    [Google Scholar]
  138. 138.  Rosenberg SM 2001. Evolving responsively: adaptive mutation. Nat. Rev. Genet. 2:504–15
    [Google Scholar]
  139. 139.  Sangurdekar DP, Zhang Z, Khodursky AB 2011. The association of DNA damage response and nucleotide level modulation with the antibacterial mechanism of the anti-folate drug trimethoprim. BMC Genom 12:583
    [Google Scholar]
  140. 140.  Schroder W, Bernhardt J, Marincola G, Klein-Hitpass L, Herbig A et al. 2014. Altering gene expression by aminocoumarins: the role of DNA supercoiling in Staphylococcus aureus. . BMC Genom 15:291
    [Google Scholar]
  141. 141.  Schroder W, Goerke C, Wolz C 2013. Opposing effects of aminocoumarins and fluoroquinolones on the SOS response and adaptability in Staphylococcus aureus. J. Antimicrob. Chemother. 68:529–38
    [Google Scholar]
  142. 142.  Shaver AC, Dombrowski PG, Sweeney JY, Treis T, Zappala RM, Sniegowski PD 2002. Fitness evolution and the rise of mutator alleles in experimental Escherichia coli populations. Genetics 162:557–66
    [Google Scholar]
  143. 143.  Sheng L, Rasco B, Zhu MJ 2016. Cinnamon oil inhibits Shiga toxin type 2 phage induction and Shiga toxin type 2 production in Escherichia coli O157:H7. Appl. Environ. Microbiol. 82:6531–40
    [Google Scholar]
  144. 144.  Simmons LA, Foti JJ, Cohen SE, Walker GC 2008. The SOS regulatory network. EcoSal Plus 2008. https://doi.org/10.1128/ecosalplus.5.4.3
    [Crossref] [Google Scholar]
  145. 145.  Sioud M, Boudabous A, Cekaite L 2009. Transcriptional responses of Bacillus subtillis and thuringiensis to antibiotics and anti-tumour drugs. Int. J. Mol. Med. 23:33–39
    [Google Scholar]
  146. 146.  Smith PA, Romesberg FE 2007. Combating bacteria and drug resistance by inhibiting mechanisms of persistence and adaptation. Nat. Chem. Biol. 3:549–56
    [Google Scholar]
  147. 147.  Song LY, Goff M, Davidian C, Mao Z, London M et al. 2016. Mutational consequences of ciprofloxacin in Escherichia coli. Antimicrob. Agents Chemother. 60:6165–72
    [Google Scholar]
  148. 148.  Tanimoto K, Tomita H, Fujimoto S, Okuzumi K, Ike Y 2008. Fluoroquinolone enhances the mutation frequency for meropenem-selected carbapenem resistance in Pseudomonas aeruginosa, but use of the high-potency drug doripenem inhibits mutant formation. Antimicrob. Agents Chemother. 52:3795–800
    [Google Scholar]
  149. 149.  Thi TD, López E, Rodríguez-Rojas A, Rodríguez-Beltrán J, Couce A et al. 2011. Effect of recA inactivation on mutagenesis of Escherichia coli exposed to sublethal concentrations of antimicrobials. J. Antimicrob. Chemother. 66:531–38
    [Google Scholar]
  150. 150.  Torres-Barcelo C, Kojadinovic M, Moxon R, MacLean RC 2015. The SOS response increases bacterial fitness, but not evolvability, under a sublethal dose of antibiotic. Proc. Biol. Sci. 282:20150885
    [Google Scholar]
  151. 151.  Vaisman A, McDonald JP, Woodgate R 2012. Translesion DNA synthesis. EcoSal Plus 2012. https://doi.org/10.1128/ecosalplus.7.2.2
    [Crossref] [Google Scholar]
  152. 152.  Valencia EY, Esposito F, Spira B, Blázquez J, Galhardo RS 2017. Ciprofloxacin-mediated mutagenesis is suppressed by subinhibitory concentrations of amikacin in Pseudomonas aeruginosa. Antimicrob. . Agents Chemother 61:e02107–16
    [Google Scholar]
  153. 153.  Veigl ML, Schneiter S, Mollis S, Sedwick WD 1991. Specificities mediated by neighboring nucleotides appear to underlie mutation induced by antifolates in E. coli. Mutat. Res. 246:75–91
    [Google Scholar]
  154. 154.  Waksman SA 1947. What is an antibiotic or an antibiotic substance?. Mycologia 39:565–69
    [Google Scholar]
  155. 155.  Wigle TJ, Lee AM, Singleton SF 2006. Conformationally selective binding of nucleotide analogues to Escherichia coli RecA: a ligand-based analysis of the RecA ATP binding site. Biochemistry 45:4502–13
    [Google Scholar]
  156. 156.  Wigle TJ, Sexton JZ, Gromova AV, Hadimani MB, Hughes MA et al. 2009. Inhibitors of RecA activity discovered by high-throughput screening: cell-permeable small molecules attenuate the SOS response in Escherichia coli. J. Biomol. Screen. 14:1092–101
    [Google Scholar]
  157. 157.  Wigle TJ, Singleton SF 2007. Directed molecular screening for RecA ATPase inhibitors. Bioorg. Med. Chem. Lett. 17:3249–53
    [Google Scholar]
  158. 158.  Witte W 1998. Medical consequences of antibiotic use in agriculture. Science 279:996–97
    [Google Scholar]
  159. 159.  Yakimov A, Pobegalov G, Bakhlanova I, Khodorkovskii M, Petukhov M, Baitin D 2017. Blocking the RecA activity and SOS-response in bacteria with a short alpha-helical peptide. Nucleic Acids Res 45:9788–96
    [Google Scholar]
  160. 160.  Yamada M, Nunoshiba T, Shimizu M, Gruz P, Kamiya H et al. 2006. Involvement of Y-family DNA polymerases in mutagenesis caused by oxidized nucleotides in Escherichia coli. J. Bacteriol. 188:4992–95
    [Google Scholar]
  161. 161.  Yang Y, Fix D 2006. Genetic analysis of the anti-mutagenic effect of genistein in Escherichia coli. Mutat. Res. 600:193–206
    [Google Scholar]
  162. 162.  Yim G, McClure J, Surette MG, Davies JE 2011. Modulation of Salmonella gene expression by subinhibitory concentrations of quinolones. J. Antibiot. 64:73–78
    [Google Scholar]
  163. 163.  Ysern P, Clerch B, Castano M, Gibert I, Barbe J, Llagostera M 1990. Induction of SOS genes in Escherichia coli and mutagenesis in Salmonella typhimurium by fluoroquinolones. Mutagenesis 5:63–66
    [Google Scholar]
/content/journals/10.1146/annurev-micro-090817-062139
Loading
/content/journals/10.1146/annurev-micro-090817-062139
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error