Multiple pathways of genome plasticity leading to development of antibiotic resistance

Antibiotics

Volumn 2, Issue 2, 2013, Pages 288-315

  Baharoglu, Zeynep ^a,b   Garriss, Geneviève ^a,b   Mazel, Didier ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

Author keywords

CRP; Horizontal gene transfer; Integron; Reactive oxygen species; RpoS; SOS; Sub MIC

Indexed keywords

AMINOGLYCOSIDE; BETA LACTAM; CEFTAZIDIME; CEPHALOSPORIN; CHLORAMPHENICOL; INTEGRASE; MACROLIDE; METRONIDAZOLE; QUINOLINE DERIVED ANTIINFECTIVE AGENT; REACTIVE OXYGEN METABOLITE; RECA PROTEIN; RIFAMPICIN; SULFAMETHOXAZOLE; SULFONAMIDE; TETRACYCLINE; TRIMETHOPRIM; VANCOMYCIN;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; CARBON SOURCE; DNA REPAIR; ESCHERICHIA COLI; GENE EXPRESSION; GENE MUTATION; GENOME; HOMOLOGOUS RECOMBINATION; HORIZONTAL GENE TRANSFER; INTEGRON; LIPID OXIDATION; MICROARRAY ANALYSIS; MINIMUM INHIBITORY CONCENTRATION; MULTIDRUG RESISTANCE; NONHUMAN; PHENOTYPE; PHYLOGENY; PRIORITY JOURNAL; REVIEW; SALMONELLA; STRESS; VIBRIO CHOLERAE;

BACTERIA (MICROORGANISMS);

EID: 84968545685     PISSN: None     EISSN: 20796382     Source Type: Journal    
DOI: 10.3390/antibiotics2020288     Document Type: Review

References (185)

1. Collis, C. M.; Kim, M. J.; Stokes, H. W.; Hall, R. M. Binding of the purified integron DNA integrase intl1 to integron-and cassette-associated recombination sites. Mol. Microbiol. 1998, 29, 477-490.
2. Biskri, L.; Bouvier, M.; Guerout, A. M.; Boisnard, S.; Mazel, D. Comparative study of class 1 integron and Vibrio cholerae superintegron integrase activities. J. Bacteriol. 2005, 187, 1740-1750.
3. Bouvier, M.; Demarre, G.; Mazel, D. Integron cassette insertion: A recombination process involving a folded single strand substrate. EMBO J. 2005, 24, 4356-4367.
4. Jove, T.; Da Re, S.; Denis, F.; Mazel, D.; Ploy, M. C. Inverse correlation between promoter strength and excision activity in class 1 integrons. PLoS Genet. 2010, 6, e1000793.
5. Mazel, D. Integrons: Agents of bacterial evolution. Nat. Rev. Microbiol. 2006, 4, 608-620.
6. Rowe-Magnus, D. A.; Mazel, D. Resistance gene capture. Curr. Opin. Microbiol. 1999, 2, 483-488.
7. Martinez-Freijo, P.; Fluit, A. C.; Schmitz, F. J.; Grek, V. S.; Verhoef, J.; Jones, M. E. Class I integrons in gram-negative isolates from different european hospitals and association with decreased susceptibility to multiple antibiotic compounds. J. Antimicrob. Chemother. 1998, 42, 689-696.
8. Stokes, H. W.; Hall, R. M. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: Integrons. Mol. Microbiol. 1989, 3, 1669-1683.
9. Liebert, C. A.; Hall, R. M.; Summers, A. O. Transposon Tn21, flagship of the floating genome. Microbiol. Mol. Biol. Rev. 1999, 63, 507-522.
10. Poirel, L.; Menuteau, O.; Agoli, N.; Cattoen, C.; Nordmann, P. Outbreak of extended-spectrum beta-lactamase veb-1-producing isolates of Acinetobacter baumannii in a French hospital. J. Clin. Microbiol. 2003, 41, 3542-3547.
11. Skurnik, D.; Ruimy, R.; Andremont, A.; Amorin, C.; Rouquet, P.; Picard, B.; Denamur, E. Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J. Antimicrob. Chemother. 2006, 57, 1215-1219.
12. Fluit, A. C.; Schmitz, F. J. Resistance integrons and super-integrons. Clin. Microbiol. Infect. 2004, 10, 272-288.
13. Rowe-Magnus, D. A.; Guerout, A. M.; Mazel, D. Bacterial resistance evolution by recruitment of super-integron gene cassettes. Mol. Microbiol. 2002, 43, 1657-1669.
14. Partridge, S. R.; Tsafnat, G.; Coiera, E.; Iredell, J. R. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol. Rev. 2009, 33, 757-784.
15. Mazel, D.; Dychinco, B.; Webb, V. A.; Davies, J. A distinctive class of integron in the Vibrio cholerae genome. Science 1998, 280, 605-608.
16. Rowe-Magnus, D. A.; Guerout, A. M.; Ploncard, P.; Dychinco, B.; Davies, J.; Mazel, D. The evolutionary history of chromosomal super-integrons provides an ancestry for multiresistant integrons. Proc. Natl. Acad. Sci. USA 2001, 98, 652-657.
17. Wu, Y. W.; Rho, M.; Doak, T. G.; Ye, Y. Oral Spirochetes implicated in dental diseases are widespread in normal human subjects and carry extremely diverse integron gene cassettes. Appl. Environ. Microbiol. 2012, 78, 5288-5296.
18. Martinez, E.; Marquez, C.; Ingold, A.; Merlino, J.; Djordjevic, S. P.; Stokes, H. W.; Chowdhury, P. R. Diverse mobilized class 1 integrons are common in the chromosomes of pathogenic Pseudomonas aeruginosa clinical isolates. Antimicrob. Agents Chemother. 2012, 56, 2169-2172.
19. Ruiz, E.; Saenz, Y.; Zarazaga, M.; Rocha-Gracia, R.; Martinez-Martinez, L.; Arlet, G.; Torres, C. Qnr, aac(6')-ib-cr and qepA genes in Escherichia coli and Klebsiella spp.: Genetic environments and plasmid and chromosomal location. J. Antimicrob. Chemother. 2012, 67, 886-897.
20. Coleman, N.; Tetu, S.; Wilson, N.; Holmes, A. An unusual integron in Treponema denticola. Microbiology 2004, 150, 3524-3526.
21. Gillings, M.; Boucher, Y.; Labbate, M.; Holmes, A.; Krishnan, S.; Holley, M.; Stokes, H. W. The evolution of class 1 integrons and the rise of antibiotic resistance. J. Bacteriol. 2008, 190, 5095-5100.
22. Le Roux, F.; Zouine, M.; Chakroun, N.; Binesse, J.; Saulnier, D.; Bouchier, C.; Zidane, N.; Ma, L.; Rusniok, C.; Lajus, A.; et al. Genome sequence of Vibrio splendidus: An abundant planctonic marine species with a large genotypic diversity. Environ. Microbiol. 2009, 11, 1959-1970.
23. Melano, R.; Petroni, A.; Garutti, A.; Saka, H. A.; Mange, L.; Pasteran, F.; Rapoport, M.; Rossi, A.; Galas, M. New carbenicillin-hydrolyzing beta-lactamase (carb-7) from Vibrio cholerae non-O1, non-O139 strains encoded by the vcr region of the V. cholerae genome. Antimicrob. Agents Chemother. 2002, 46, 2162-2168.
24. Petroni, A.; Melano, R. G.; Saka, H. A.; Garutti, A.; Mange, L.; Pasteran, F.; Rapoport, M.; Miranda, M.; Faccone, D.; Rossi, A.; et al. Carb-9, a carbenicillinase encoded in the vcr region of Vibrio cholerae non-O1, non-O139 belongs to a family of cassette-encoded beta-lactamases. Antimicrob. Agents Chemother. 2004, 48, 4042-4046.
25. Fonseca, E. L.; Dos Santos Freitas, F.; Vieira, V. V.; Vicente, A. C. New qnr gene cassettes associated with superintegron repeats in Vibrio cholerae O1. Emerg. Infect. Dis. 2008, 14, 1129-1131.
26. Gassama Sow, A.; Aidara-Kane, A.; Barraud, O.; Gatet, M.; Denis, F.; Ploy, M. C. High prevalence of trimethoprim-resistance cassettes in class 1 and 2 integrons in senegalese shigella spp isolates. J. Infect. Dev. Ctries. 2010, 4, 207-212.
27. Walker, G. C. The SOS Response of Escherichia coli. In Escherichia coli and Salmonella: Cellular and Molecular Biology; Neidhardt, F. C., Curtiss, R., III, Ingraham, J. L., Lin, E. C. C., Low, K. B., Magasanik, B., Reznikoff, W. S., Riley, M., Schaechter, M., Umbarger, H. E., Eds.; American Society of Microbiology: Washington, DC, USA, 1996; pp. 1400-1416.
28. Wade, J. T.; Reppas, N. B.; Church, G. M.; Struhl, K. Genomic analysis of LlexA binding reveals the permissive nature of the Escherichia coli genome and identifies unconventional target sites. Genes. Dev. 2005, 19, 2619-2630.
29. Guerin, E.; Cambray, G.; Sanchez-Alberola, N.; Campoy, S.; Erill, I.; Da Re, S.; Gonzalez-Zorn, B.; Barbe, J.; Ploy, M. C.; Mazel, D. The SOS response controls integron recombination. Science 2009, 324, 1034.
30. Cambray, G.; Sanchez-Alberola, N.; Campoy, S.; Guerin, E.; Da Re, S.; Gonzalez-Zorn, B.; Ploy, M. C.; Barbe, J.; Mazel, D.; Erill, I. Prevalence of SOS-mediated control of integron integrase expression as an adaptive trait of chromosomal and mobile integrons. Mob. DNA 2011, 2, e6.
31. Baharoglu, Z.; Krin, E.; Mazel, D. Transformation-induced SOS regulation and carbon catabolite control of the V. cholerae integron integrase: Connecting environment and genome plasticity. J. Bacteriol. 2012, doi: 10. 1128/JB. 05982-11.
32. Boucher, Y.; Cordero, O. X.; Takemura, A.; Hunt, D. E.; Schliep, K.; Bapteste, E.; Lopez, P.; Tarr, C. L.; Polz, M. F. Local mobile gene pools rapidly cross species boundaries to create endemicity within global Vibrio cholerae populations. MBio 2011, 2, e00335-10.
33. Baharoglu, Z.; Bikard, D.; Mazel, D. Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet. 2010, 6, e1001165.
34. Matic, I.; Rayssiguier, C.; Radman, M. Interspecies gene exchange in bacteria: The role of SOS and mismatch repair systems in evolution of species. Cell 1995, 80, 507-515.
35. Matic, I.; Taddei, F.; Radman, M. No genetic barriers between Salmonella enterica serovar typhimurium and Escherichia coli in SOS-induced mismatch repair-deficient cells. J. Bacteriol. 2000, 182, 5922-5924.
36. Delmas, S.; Matic, I. Cellular response to horizontally transferred DNA in Escherichia coli is tuned by DNA repair systems. DNA Repair 2005, 4, 221-229.
37. Smorawinska, M.; Szuplewska, M.; Zaleski, P.; Wawrzyniak, P.; Maj, A.; Plucienniczak, A.; Bartosik, D. Mobilizable narrow host range plasmids as natural suicide vectors enabling horizontal gene transfer among distantly related bacterial species. FEMS Microbiol. Lett. 2012, 326, 76-82.
38. Colwell, R. R. A Global and Historical Perspective of the Genus Vibrio. In The Biology of Vibrios; Thompson, F. L., Ed.; ASM Press: Washington, DC, USA, 2006.
39. Urakawa, H.; Rivera, I. N. G. Aquatic Environment. In The Biology of Vibrios; Thompson, F. L., Ed.; ASM Press: Washington, DC, USA, 2006.
40. Bryan, L. E.; Shahrabadi, M. S.; van den Elzen, H. M. Gentamicin resistance in Pseudomonas aeruginosa: R-factor-mediated resistance. Antimicrob. Agents Chemother. 1974, 6, 191-199.
41. Kontomichalou, P.; Mitani, M.; Clowes, R. C. Circular R-factor molecules controlling penicillinase synthesis, replicating in Escherichia coli under either relaxed or stringent control. J. Bacteriol. 1970, 104, 34-44.
42. Moura, A.; Henriques, I.; Smalla, K.; Correia, A. Wastewater bacterial communities bring together broad-host range plasmids, integrons and a wide diversity of uncharacterized gene cassettes. Res. Microbiol. 2010, 161, 58-66.
43. Moura, A.; Oliveira, C.; Henriques, I.; Smalla, K.; Correia, A. Broad diversity of conjugative plasmids in integron-carrying bacteria from wastewater environments. FEMS Microbiol. Lett. 2012, 330, 157-164.
44. Stecher, B.; Denzler, R.; Maier, L.; Bernet, F.; Sanders, M. J.; Pickard, D. J.; Barthel, M.; Westendorf, A. M.; Krogfelt, K. A.; Walker, A. W.; et al. Gut inflammation can boost horizontal gene transfer between pathogenic and commensal Enterobacteriaceae. Proc. Natl. Acad. Sci. USA 2012, 109, 1269-1274.
45. Dubnau, D. DNA uptake in bacteria. Annu. Rev. Microbiol. 1999, 53, 217-244.
46. Claverys, J. P.; Martin, B.; Polard, P. The genetic transformation machinery: Composition, localization, and mechanism. FEMS Microbiol. Rev. 2009, 33, 643-656.
47. Yasbin, R. E.; Wilson, G. A.; Young, F. E. Transformation and transfection in lysogenic strains of Bacillus subtilis: Evidence for selective induction of prophage in competent cells. J. Bacteriol. 1975, 121, 296-304.
48. Seitz, P.; Blokesch, M. Cues and regulatory pathways involved in natural competence and transformation in pathogenic and environmental gram-negative bacteria. FEMS Microbiol. Rev. 2012, 37, 336-363.
49. Charpentier, X.; Polard, P.; Claverys, J. P. Induction of competence for genetic transformation by antibiotics: Convergent evolution of stress responses in distant bacterial species lacking SOS? Curr. Opin. Microbiol. 2012, 15, 570-576.
50. Meibom, K. L.; Blokesch, M.; Dolganov, N. A.; Wu, C. Y.; Schoolnik, G. K. Chitin induces natural competence in Vibrio cholerae. Science 2005, 310, 1824-1827.
51. Lo Scrudato, M.; Blokesch, M. The regulatory network of natural competence and transformation of Vibrio cholerae. PLoS Genet. 2012, 8, e1002778.
52. Zulty, J. J.; Barcak, G. J. Identification of a DNA transformation gene required for com101a+ expression and supertransformer phenotype in Haemophilus influenzae. Proc. Natl. Acad. Sci. USA 1995, 92, 3616-3620.
53. Yamamoto, S.; Morita, M.; Izumiya, H.; Watanabe, H. Chitin disaccharide (Glcnac)(2) induces natural competence in Vibrio cholerae through transcriptional and translational activation of a positive regulatory gene tfoX(vc). Gene 2010, 457, 42-49.
54. Karudapuram, S.; Barcak, G. J. The haemophilus influenzae dprABC genes constitute a competence-inducible operon that requires the product of the tfoX (sxy) gene for transcriptional activation. J. Bacteriol. 1997, 179, 4815-4820.
55. Cameron, A. D.; Volar, M.; Bannister, L. A.; Redfield, R. J. RNA secondary structure regulates the translation of sxy and competence development in Haemophilus influenzae. Nucleic Acids Res. 2008, 36, 10-20.
56. Bosse, J. T.; Sinha, S.; Schippers, T.; Kroll, J. S.; Redfield, R. J.; Langford, P. R. Natural competence in strains of Actinobacillus pleuropneumoniae. FEMS Microbiol. Lett. 2009, 298, 124-130.
57. Redfield, R. J.; Cameron, A. D.; Qian, Q.; Hinds, J.; Ali, T. R.; Kroll, J. S.; Langford, P. R. A novel CRP-dependent regulon controls expression of competence genes in Haemophilus influenzae. J. Mol. Biol. 2005, 347, 735-747.
58. Meibom, K. L.; Li, X. B.; Nielsen, A. T.; Wu, C. Y.; Roseman, S.; Schoolnik, G. K. The Vibrio cholerae chitin utilization program. Proc. Natl. Acad. Sci. USA 2004, 101, 2524-2529.
59. Blokesch, M.; Schoolnik, G. K. The extracellular nuclease Dns and its role in natural transformation of Vibrio cholerae. J. Bacteriol. 2008, 190, 7232-7240.
60. Domingues, S.; Harms, K.; Fricke, W. F.; Johnsen, P. J.; da Silva, G. J.; Nielsen, K. M. Natural transformation facilitates transfer of transposons, integrons and gene cassettes between bacterial species. PLoS Pathog. 2012, 8, e1002837.
61. Singletary, L. A.; Gibson, J. L.; Tanner, E. J.; McKenzie, G. J.; Lee, P. L.; Gonzalez, C.; Rosenberg, S. M. An SOS-regulated type 2 toxin-antitoxin system. J. Bacteriol. 2009, 191, 7456-7465.
62. Pandey, D. P.; Gerdes, K. Toxin-antitoxin loci are highly abundant in free-living but lost from host-associated prokaryotes. Nucleic Acids Res. 2005, 33, 966-976.
63. Hochhut, B.; Lotfi, Y.; Mazel, D.; Faruque, S. M.; Woodgate, R.; Waldor, M. K. Molecular analysis of antibiotic resistance gene clusters in Vibrio cholerae O139 and O1 SXT constins. Antimicrob. Agents Chemother. 2001, 45, 2991-3000.
64. Wozniak, R. A.; Fouts, D. E.; Spagnoletti, M.; Colombo, M. M.; Ceccarelli, D.; Garriss, G.; Dery, C.; Burrus, V.; Waldor, M. K. Comparative ICE genomics: Insights into the evolution of the SXT/R391 family of ICEs. PLoS Genet. 2009, 5, e1000786.
65. Toleman, M. A.; Bennett, P. M.; Walsh, T. R. ISCR elements: Novel gene-capturing systems of the 21st century? Microbiol. Mol. Biol. Rev. 2006, 70, 296-316.
66. Baharoglu, Z.; Mazel, D. Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics, a route towards multi-resistance. Antimicrob. Agents Chemother. 2011, 55, 2438-2441.
67. Wozniak, R. A.; Waldor, M. K. Integrative and conjugative elements: Mosaic mobile genetic elements enabling dynamic lateral gene flow. Nat. Rev. Microbiol. 2010, 8, 552-563.
68. Garriss, G.; Burrus, V. Integrating Conjugative Elements of the SXT/R391 Family. In Bacterial Integrative Mobile Genetic Elements; Roberts, A. P., Mullany, P., Eds.; Landes Bioscience: Austin, TX, USA, 2013.
69. Wozniak, R. A.; Waldor, M. K. A toxin-antitoxin system promotes the maintenance of an integrative conjugative element. PLoS Genet. 2009, 5, e1000439.
70. Dziewit, L.; Jazurek, M.; Drewniak, L.; Baj, J.; Bartosik, D. The SXT conjugative element and linear prophage N15 encode toxin-antitoxin-stabilizing systems homologous to the tad-ata module of the Paracoccus aminophilus plasmid pAMI2. J. Bacteriol. 2007, 189, 1983-1997.
71. Bordeleau, E.; Brouillette, E.; Robichaud, N.; Burrus, V. Beyond antibiotic resistance: Integrating conjugative elements of the SXT/R391 family that encode novel diguanylate cyclases participate to c-di-GMP signalling in Vibrio cholerae. Environ. Microbiol. 2009, 12, 510-523.
72. Faruque, S. M.; Biswas, K.; Udden, S. M.; Ahmad, Q. S.; Sack, D. A.; Nair, G. B.; Mekalanos, J. J. Transmissibility of cholera: In vivo-formed biofilms and their relationship to infectivity and persistence in the environment. Proc. Natl. Acad. Sci. USA 2006, 103, 6350-6355.
73. Butler, S. M.; Camilli, A. Both chemotaxis and net motility greatly influence the infectivity of vibrio cholerae. Proc. Natl. Acad. Sci. USA 2004, 101, 5018-5023.
74. Beaber, J. W.; Hochhut, B.; Waldor, M. K. SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 2004, 427, 72-74.
75. Burrus, V.; Waldor, M. K. Control of SXT integration and excision. J. Bacteriol. 2003, 185, 5045-5054.
76. Cambray, G.; Guerout, A. M.; Mazel, D. Integrons. Annu. Rev. Genet. 2010, 44, 141-166.
77. Garriss, G.; Waldor, M. K.; Burrus, V. Mobile antibiotic resistance encoding elements promote their own diversity. PLoS Genet. 2009, 5, e1000775.
78. Garriss, G.; Poulin-Laprade, D.; Burrus, V. DNA damaging agents induce the RecA-independent homologous recombination functions of integrating conjugative elements of the SXT/R391 family. J. Bacteriol. 2013, 195, 1991-2003.
79. Hochhut, B.; Beaber, J. W.; Woodgate, R.; Waldor, M. K. Formation of chromosomal tandem arrays of the SXT element and R391, two conjugative chromosomally integrating elements that share an attachment site. J. Bacteriol. 2001, 183, 1124-1132.
80. Burrus, V.; Waldor, M. K. Formation of SXT tandem arrays and SXT-R391 hybrids. J. Bacteriol. 2004, 186, 2636-2645.
81. Galimand, M.; Guiyoule, A.; Gerbaud, G.; Rasoamanana, B.; Chanteau, S.; Carniel, E.; Courvalin, P. Multidrug resistance in Yersinia pestis mediated by a transferable plasmid. N. Engl. J. Med. 1997, 337, 677-680.
82. Lindsey, R. L.; Fedorka-Cray, P. J.; Frye, J. G.; Meinersmann, R. J. IncA/C plasmids are prevalent in multidrug-resistant Salmonella enterica isolates. Appl. Environ. Microbiol. 2009, 75, 1908-1915.
83. Fricke, W. F.; Welch, T. J.; McDermott, P. F.; Mammel, M. K.; LeClerc, J. E.; White, D. G.; Cebula, T. A.; Ravel, J. Comparative genomics of the IncA/C multidrug resistance plasmid family. J. Bacteriol. 2009, 191, 4750-4757.
84. Pan, J. C.; Ye, R.; Wang, H. Q.; Xiang, H. Q.; Zhang, W.; Yu, X. F.; Meng, D. M.; He, Z. S. Vibrio cholerae O139 multiple-drug resistance mediated by Yersinia pestis pIP1202-like conjugative plasmids. Antimicrob. Agents Chemother. 2008, 52, 3829-3836.
85. Welch, T. J.; Fricke, W. F.; McDermott, P. F.; White, D. G.; Rosso, M. L.; Rasko, D. A.; Mammel, M. K.; Eppinger, M.; Rosovitz, M. J.; Wagner, D.; et al. Multiple antimicrobial resistance in plague: An emerging public health risk. PLoS One 2007, 2, e309.
86. Carattoli, A.; Villa, L.; Poirel, L.; Bonnin, R. A.; Nordmann, P. Evolution of IncA/C blacmy-2-carrying plasmids by acquisition of the blandm-1 carbapenemase gene. Antimicrob. Agents Chemother. 2011, 56, 783-786.
87. Johnson, T. J.; Lang, K. S. IncA/C plasmids: An emerging threat to human and animal health? Mob. Genet. Elem. 2012, 2, 55-58.
88. Bruckner, R.; Titgemeyer, F. Carbon catabolite repression in bacteria: Choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol. Lett. 2002, 209, 141-148.
89. Kolb, A.; Busby, S.; Buc, H.; Garges, S.; Adhya, S. Transcriptional regulation by cAMP and its receptor protein. Annu. Rev. Biochem. 1993, 62, 749-795.
90. Stulke, J.; Hillen, W. Carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 1999, 2, 195-201.
91. Cameron, A. D.; Redfield, R. J. Non-canonical crp sites control competence regulons in Escherichia coli and many other gamma-proteobacteria. Nucleic Acids Res. 2006, 34, 6001-6014.
92. de Crombrugghe, B.; Busby, S.; Buc, H. Cyclic AMP receptor protein: Role in transcription activation. Science 1984, 224, 831-838.
93. Rojo, F. Carbon catabolite repression in Pseudomonas: Optimizing metabolic versatility and interactions with the environment. FEMS Microbiol. Rev. 2010, 34, 658-684.
94. Gorke, B.; Stulke, J. Carbon catabolite repression in bacteria: Many ways to make the most out of nutrients. Nat. Rev. Microbiol. 2008, 6, 613-624.
95. Gosset, G.; Zhang, Z.; Nayyar, S.; Cuevas, W. A.; Saier, M. H., Jr. Transcriptome analysis of CRP-dependent catabolite control of gene expression in Escherichia coli. J. Bacteriol. 2004, 186, 3516-3524.
96. Liang, W.; Pascual-Montano, A.; Silva, A. J.; Benitez, J. A. The cyclic AMP receptor protein modulates quorum sensing, motility and multiple genes that affect intestinal colonization in Vibrio cholerae. Microbiology 2007, 153, 2964-2975.
97. Zheng, D.; Constantinidou, C.; Hobman, J. L.; Minchin, S. D. Identification of the CRP regulon using in vitro and in vivo transcriptional profiling. Nucleic Acids Res. 2004, 32, 5874-5893.
98. Kumar, S.; Srivastava, S. Cyclic AMP and its receptor protein are required for expression of transfer genes of conjugative plasmid f in Escherichia coli. Mol. Gen. Genet. 1983, 190, 27-34.
99. Skorupski, K.; Taylor, R. K. Cyclic AMP and its receptor protein negatively regulate the coordinate expression of cholera toxin and toxin-coregulated pilus in Vibrio cholerae. Proc. Natl. Acad. Sci. USA 1997, 94, 265-270.
100. Silva, A. J.; Benitez, J. A. Transcriptional regulation of Vibrio cholerae hemagglutinin/protease by the cyclic AMP receptor protein and RpoS. J. Bacteriol. 2004, 186, 6374-6382.
101. Sinha, S.; Cameron, A. D.; Redfield, R. J. Sxy induces a crp-s regulon in Escherichia coli. J. Bacteriol. 2009, 191, 5180-5195.
102. Sinha, S.; Mell, J. C.; Redfield, R. J. Seventeen Sxy-dependent cyclic AMP receptor protein site-regulated genes are needed for natural transformation in Haemophilus influenzae. J. Bacteriol. 2012, 194, 5245-5254.
103. Blokesch, M. Chitin colonization, chitin degradation and chitin-induced natural competence of Vibrio cholerae are subject to catabolite repression. Environ. Microbiol. 2012, 14, 1898-1912.
104. Botsford, J. L.; Harman, J. G. Cyclic AMP in prokaryotes. Microbiol. Rev. 1992, 56, 100-122.
105. Liu, Y. C.; Huang, W. K.; Huang, T. S.; Kunin, C. M. Detection of antimicrobial activity in urine for epidemiologic studies of antibiotic use. J. Clin. Epidemiol. 1999, 52, 539-545.
106. Haggard, B. E.; Bartsch, L. D. Net changes in antibiotic concentrations downstream from an effluent discharge. J. Environ. Qual. 2009, 38, 343-352.
107. Fick, J.; Soderstrom, H.; Lindberg, R. H.; Phan, C.; Tysklind, M.; Larsson, D. G. Contamination of surface, ground, and drinking water from pharmaceutical production. Environ. Toxicol. Chem. 2009, 28, 2522-2527.
108. Kummerer, K. Antibiotics in the aquatic environment-A review-Part I. Chemosphere 2009, 75, 417-434.
109. Kummerer, K. Antibiotics in the aquatic environment-A review-Part II. Chemosphere 2009, 75, 435-441.
110. Hughes, D.; Andersson, D. I. Selection of resistance at lethal and non-lethal antibiotic concentrations. Curr. Opin. Microbiol. 2012, 15, 555-560.
111. Goh, E. B.; Yim, G.; Tsui, W.; McClure, J.; Surette, M. G.; Davies, J. Transcriptional modulation of bacterial gene expression by subinhibitory concentrations of antibiotics. Proc. Natl. Acad. Sci. USA 2002, 99, 17025-17030.
112. Bernier, S. P.; Surette, M. G. Concentration-dependent activity of antibiotics in natural environments. Front. Microbiol. 2013, 4, e20.
113. Davies, J.; Spiegelman, G. B.; Yim, G. The world of subinhibitory antibiotic concentrations. Curr. Opin. Microbiol. 2006, 9, 445-453.
114. Yim, G.; de la Cruz, F.; Spiegelman, G. B.; Davies, J. Transcription modulation of Salmonella enterica serovar typhimurium promoters by sub-mic levels of rifampin. J. Bacteriol. 2006, 188, 7988-7991.
115. Yim, G.; McClure, J.; Surette, M. G.; Davies, J. E. Modulation of Salmonella gene expression by subinhibitory concentrations of quinolones. J. Antibiot. (Tokyo) 2011, 64, 73-78.
116. Tsui, W. H.; Yim, G.; Wang, H. H.; McClure, J. E.; Surette, M. G.; Davies, J. Dual effects of Mls antibiotics: Transcriptional modulation and interactions on the ribosome. Chem. Biol. 2004, 11, 1307-1316.
117. Linares, J. F.; Gustafsson, I.; Baquero, F.; Martinez, J. L. Antibiotics as intermicrobial signaling agents instead of weapons. Proc. Natl. Acad. Sci. USA 2006, 103, 19484-19489.
118. Kaplan, J. B. Antibiotic-induced biofilm formation. Int. J. Artif. Organs 2011, 34, 737-751.
119. Kaplan, J. B.; Jabbouri, S.; Sadovskaya, I. Extracellular DNA-dependent biofilm formation by Staphylococcus epidermidis rp62a in response to subminimal inhibitory concentrations of antibiotics. Res. Microbiol. 2011, 162, 535-541.
120. Haddadin, R. N.; Saleh, S.; Al-Adham, I. S.; Buultjens, T. E.; Collier, P. J. The effect of subminimal inhibitory concentrations of antibiotics on virulence factors expressed by Staphylococcus aureus biofilms. J. Appl. Microbiol. 2010, 108, 1281-1291.
121. Hoffman, L. R.; D'Argenio, D. A.; MacCoss, M. J.; Zhang, Z.; Jones, R. A.; Miller, S. I. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005, 436, 1171-1175.
122. Rogers, S. A.; Huigens, R. W., 3rd; Cavanagh, J.; Melander, C. Synergistic effects between conventional antibiotics and 2-aminoimidazole-derived antibiofilm agents. Antimicrob. Agents Chemother. 2010, 54, 2112-2118.
123. Bernier, S. P.; Lebeaux, D.; Defrancesco, A. S.; Valomon, A.; Soubigou, G.; Coppee, J. Y.; Ghigo, J. M.; Beloin, C. Starvation, together with the SOS response, mediates high biofilm-specific tolerance to the fluoroquinolone ofloxacin. PLoS Genet. 2013, 9, e1003144.
124. Mueller, R. S.; Dill, B. D.; Pan, C.; Belnap, C. P.; Thomas, B. C.; VerBerkmoes, N. C.; Hettich, R. L.; Banfield, J. F. Proteome changes in the initial bacterial colonist during ecological succession in an acid mine drainage biofilm community. Environ. Microbiol. 2011, 13, 2279-2292.
125. Gotoh, H.; Kasaraneni, N.; Devineni, N.; Dallo, S. F.; Weitao, T. SOS involvement in stress-inducible biofilm formation. Biofouling 2010, 26, 603-611.
126. Molin, S.; Tolker-Nielsen, T. Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr. Opin. Biotechnol. 2003, 14, 255-261.
127. Hennequin, C.; Aumeran, C.; Robin, F.; Traore, O.; Forestier, C. Antibiotic resistance and plasmid transfer capacity in biofilm formed with a CTX-M-15-producing Klebsiella pneumoniae isolate. J. Antimicrob. Chemother. 2012, 67, 2123-2130.
128. Ysern, P.; Clerch, B.; Castano, M.; Gibert, I.; Barbe, J.; Llagostera, M. Induction of SOS genes in Escherichia coli and mutagenesis in Salmonella typhimurium by fluoroquinolones. Mutagenesis 1990, 5, 63-66.
129. Miller, C.; Thomsen, L. E.; Gaggero, C.; Mosseri, R.; Ingmer, H.; Cohen, S. N. SOS response induction by beta-lactams and bacterial defense against antibiotic lethality. Science 2004, 305, 1629-1631.
130. Perez-Capilla, T.; Baquero, M. R.; Gomez-Gomez, J. M.; Ionel, A.; Martin, S.; Blazquez, J. SOS-independent induction of dinB transcription by beta-lactam-mediated inhibition of cell wall synthesis in Escherichia coli. J. Bacteriol. 2005, 187, 1515-1518.
131. Shaw, K. J.; Miller, N.; Liu, X.; Lerner, D.; Wan, J.; Bittner, A.; Morrow, B. J. Comparison of the changes in global gene expression of Escherichia coli induced by four bactericidal agents. J. Mol. Microbiol. Biotechnol. 2003, 5, 105-122.
132. Mesak, L. R.; Davies, J. Phenotypic changes in ciprofloxacin-resistant Staphylococcus aureus. Res. Microbiol. 2009, 160, 785-791.
133. Mesak, L. R.; Miao, V.; Davies, J. Effects of subinhibitory concentrations of antibiotics on SOS and DNA repair gene expression in Staphylococcus aureus. Antimicrob. Agents Chemother. 2008, 52, 3394-3397.
134. Lopez, E.; Blazquez, J. Effect of subinhibitory concentrations of antibiotics on intrachromosomal homologous recombination in Escherichia coli. Antimicrob. Agents Chemother. 2009, 53, 3411-3415.
135. Cirz, R. T.; Romesberg, F. E. Induction and inhibition of ciprofloxacin resistance-conferring mutations in hypermutator bacteria. Antimicrob. Agents Chemother. 2006, 50, 220-225.
136. Didier, J. P.; Villet, R.; Huggler, E.; Lew, D. P.; Hooper, D. C.; Kelley, W. L.; Vaudaux, P. Impact of ciprofloxacin exposure on Staphylococcus aureus genomic alterations linked with emergence of rifampin resistance. Antimicrob. Agents Chemother. 2011, 55, 1946-1952.
137. Cohen, S. E.; Walker, G. C. The transcription elongation factor NusA is required for stress-induced mutagenesis in Escherichia coli. Curr. Biol. 2010, 20, 80-85.
138. Baharoglu, Z.; Krin, E.; Mazel, D. RpoS plays a central role in the SOS induction by sub-lethal aminoglycoside concentrations in Vibrio cholerae. PLoS Genet. 2013, 9, e1003421.
139. Hocquet, D.; Llanes, C.; Thouverez, M.; Kulasekara, H. D.; Bertrand, X.; Plesiat, P.; Mazel, D.; Miller, S. I. Evidence for induction of integron-based antibiotic resistance by the SOS response in a clinical setting. PLoS Pathog. 2012, 8, e1002778.
140. Erill, I.; Campoy, S.; Barbe, J. Aeons of distress: An evolutionary perspective on the bacterial SOS response. FEMS Microbiol. Rev. 2007, 31, 637-656.
141. Gutierrez, A.; Laureti, L.; Crussard, S.; Abida, H.; Rodríguez Rojas, A.; Blázquez, J.; Baharoglu, Z.; Mazel, D.; Darfeuille, F.; Vogel, J.; et al. α-lactam antibiotics promote mutagenesis via RpoS-mediated replication fidelity reduction. Nat. Commun. 2013, 4, e1610.
142. Denamur, E.; Tenaillon, O.; Deschamps, C.; Skurnik, D.; Ronco, E.; Gaillard, J. L.; Picard, B.; Branger, C.; Matic, I. Intermediate mutation frequencies favor evolution of multidrug resistance in Escherichia coli. Genetics 2005, 171, 825-827.
143. Da Re, S.; Garnier, F.; Guerin, E.; Campoy, S.; Denis, F.; Ploy, M. C. The SOS response promotes qnrB quinolone-resistance determinant expression. EMBO Rep. 2009, 10, 929-933.
144. Ubeda, C.; Maiques, E.; Knecht, E.; Lasa, I.; Novick, R. P.; Penades, J. R. Antibiotic-induced SOS response promotes horizontal dissemination of pathogenicity island-encoded virulence factors in Staphylococci. Mol. Microbiol. 2005, 56, 836-844.
145. Maiques, E.; Ubeda, C.; Campoy, S.; Salvador, N.; Lasa, I.; Novick, R. P.; Barbe, J.; Penades, J. R. Beta-lactam antibiotics induce the SOS response and horizontal transfer of virulence factors in Staphylococcus aureus. J. Bacteriol. 2006, 188, 2726-2729.
146. Prudhomme, M.; Attaiech, L.; Sanchez, G.; Martin, B.; Claverys, J. P. Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae. Science 2006, 313, 89-92.
147. Gullberg, E.; Cao, S.; Berg, O. G.; Ilback, C.; Sandegren, L.; Hughes, D.; Andersson, D. I. Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog. 2011, 7, e1002158.
148. Gustafsson, I.; Sjolund, M.; Torell, E.; Johannesson, M.; Engstrand, L.; Cars, O.; Andersson, D. I. Bacteria with increased mutation frequency and antibiotic resistance are enriched in the commensal flora of patients with high antibiotic usage. J. Antimicrob. Chemother. 2003, 52, 645-650.
149. Liu, A.; Fong, A.; Becket, E.; Yuan, J.; Tamae, C.; Medrano, L.; Maiz, M.; Wahba, C.; Lee, C.; Lee, K.; et al. Selective advantage of resistant strains at trace levels of antibiotics: A simple and ultrasensitive color test for detection of antibiotics and genotoxic agents. Antimicrob. Agents Chemother. 2011, 55, 1204-1210.
150. Dorr, T.; Lewis, K.; Vulic, M. SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet. 2009, 5, e1000760.
151. Dorr, T.; Vulic, M.; Lewis, K. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol. 2010, 8, e1000317.
152. Lewis, K. Persister cells. Annu. Rev. Microbiol. 2010, 64, 357-372.
153. Guerout, A. M.; Iqbal, N.; Mine, N.; Ducos-Galand, M.; van Melderen, L.; Mazel, D. Characterization of the phd-doc and ccd toxin-antitoxin cassettes from Vibrio superintegrons. J. Bacteriol. 2013, 195, 2270-2283.
154. Kohanski, M. A.; DePristo, M. A.; Collins, J. J. Sublethal antibiotic treatment leads to multidrug resistance via radical-induced mutagenesis. Mol. Cell 2010, 37, 311-320.
155. Mcbride, T. J.; Preston, B. D.; Loeb, L. A. Mutagenic spectrum resulting from DNA damage by oxygen radicals. Biochemistry 1991, 30, 207-213.
156. Nunoshiba, T.; Obata, F.; Boss, A. C.; Oikawa, S.; Mori, T.; Kawanishi, S.; Yamamoto, E. Role of iron and superoxide for generation of hydroxyl radical, oxidative DNA lesions, and mutagenesis in Escherichia coli. J. Biol. Chem. 1999, 274, 34832-34837.
157. Fraud, S.; Poole, K. Oxidative stress induction of the mexXY multidrug efflux genes and promotion of aminoglycoside resistance development in Pseudomonas aeruginosa. Antimicrob. Agents Chemother. 2011, 55, 1068-1074.
158. Aiassa, V.; Barnes, A. I.; Smania, A. M.; Albesa, I. Sublethal ciprofloxacin treatment leads to resistance via antioxidant systems in Proteus mirabilis. FEMS Microbiol. Lett. 2012, 327, 25-32.
159. Dwyer, D. J.; Kohanski, M. A.; Collins, J. J. Role of reactive oxygen species in antibiotic action and resistance. Curr. Opin. Microbiol. 2009, 12, 482-489.
160. Dwyer, D. J.; Kohanski, M. A.; Hayete, B.; Collins, J. J. Gyrase inhibitors induce an oxidative damage cellular death pathway in Escherichia coli. Mol. Syst. Biol. 2007, 3, e91.
161. Wholey, W. Y.; Jakob, U. Hsp33 confers bleach resistance by protecting elongation factor Tu against oxidative degradation in Vibrio cholerae. Mol. Microbiol. 2012, 83, 981-991.
162. Nguyen, D.; Joshi-Datar, A.; Lepine, F.; Bauerle, E.; Olakanmi, O.; Beer, K.; McKay, G.; Siehnel, R.; Schafhauser, J.; Wang, Y.; et al. Active starvation responses mediate antibiotic tolerance in biofilms and nutrient-limited bacteria. Science 2011, 334, 982-986.
163. Shatalin, K.; Shatalina, E.; Mironov, A.; Nudler, E. H2S: A universal defense against antibiotics in bacteria. Science 2011, 334, 986-990.
164. Belenky, P.; Collins, J. J. Microbiology. Antioxidant strategies to tolerate antibiotics. Science 2011, 334, 915-916.
165. Allen, K. J.; Griffiths, M. W. Impact of hydroxyl-and superoxide anion-based oxidative stress on logarithmic and stationary phase Escherichia coli O157: H7 stress and virulence gene expression. Food Microbiol. 2012, 29, 141-147.
166. Merrikh, H.; Ferrazzoli, A. E.; Bougdour, A.; Olivier-Mason, A.; Lovett, S. T. A DNA damage response in Escherichia coli involving the alternative sigma factor, RpoS. Proc. Natl. Acad. Sci. USA 2009, 106, 611-616.
167. Merrikh, H.; Ferrazzoli, A. E.; Lovett, S. T. Growth phase and (p)ppGpp control of IraD, a regulator of RpoS stability, in Escherichia coli. J. Bacteriol. 2009, 191, 7436-7446.
168. Battesti, A.; Tsegaye, Y. M.; Packer, D. G.; Majdalani, N.; Gottesman, S. H-NS regulation of IraD and IraM anti-adaptors for control of RpoS degradation. J. Bacteriol. 2012, 194, 2470-2478.
169. Hengge-Aronis, R. Signal transduction and regulatory mechanisms involved in control of the sigma(S) (RpoS) subunit of RNA polymerase. Microbiol. Mol. Biol. Rev. 2002, 66, 373-395.
170. Barth, E.; Gora, K. V.; Gebendorfer, K. M.; Settele, F.; Jakob, U.; Winter, J. Interplay of cellular cAMP levels, {sigma}S activity and oxidative stress resistance in Escherichia coli. Microbiology 2009, 155, 1680-1689.
171. Daly, M. J. A new perspective on radiation resistance based on Deinococcus radiodurans. Nat. Rev. Microbiol. 2009, 7, 237-245.
172. Henle, E. S.; Linn, S. Formation, prevention, and repair of DNA damage by iron/hydrogen peroxide. J. Biol. Chem. 1997, 272, 19095-19098.
173. Keyer, K.; Imlay, J. A. Superoxide accelerates DNA damage by elevating free-iron levels. Proc. Natl. Acad. Sci. USA 1996, 93, 13635-13640.
174. Hansen, S.; Lewis, K.; Vulic, M. Role of global regulators and nucleotide metabolism in antibiotic tolerance in Escherichia coli. Antimicrob. Agents Chemother. 2008, 52, 2718-2726.
175. Miyazaki, R.; Minoia, M.; Pradervand, N.; Sulser, S.; Reinhard, F.; van der Meer, J. R. Cellular variability of RpoS expression underlies subpopulation activation of an integrative and conjugative element. PLoS Genet. 2012, 8, e1002818.
176. Santos-Zavaleta, A.; Gama-Castro, S.; Perez-Rueda, E. A comparative genome analysis of the RpoS sigmulon shows a high diversity of responses and origins. Microbiology 2011, 157, 1393-1401.
177. Chiang, S. M.; Schellhorn, H. E. Evolution of the RpoS regulon: Origin of RpoS and the conservation of RpoS-dependent regulation in bacteria. J. Mol. Evol. 2010, 70, 557-571.
178. King, T.; Seeto, S.; Ferenci, T. Genotype-by-environment interactions influencing the emergence of RpoS mutations in Escherichia coli populations. Genetics 2006, 172, 2071-2079.
179. Zambrano, M. M.; Siegele, D. A.; Almiron, M.; Tormo, A.; Kolter, R. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 1993, 259, 1757-1760.
180. Zhang, Y.; Shi, C.; Yu, J.; Ren, J.; Sun, D. RpoS regulates a novel type of plasmid DNA transfer in Escherichia coli. PLoS One 2012, 7, e33514.
181. Joelsson, A.; Kan, B.; Zhu, J. Quorum sensing enhances the stress response in Vibrio cholerae. Appl. Environ. Microbiol. 2007, 73, 3742-3746.
182. Allison, K. R.; Brynildsen, M. P.; Collins, J. J. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 2011, 473, 216-220.
183. Farha, M. A.; Brown, E. D. Discovery of antibiotic adjuvants. Nat. Biotechnol. 2013, 31, 120-122.
184. Brynildsen, M. P.; Winkler, J. A.; Spina, C. S.; Macdonald, I. C.; Collins, J. J. Potentiating antibacterial activity by predictably enhancing endogenous microbial ROS production. Nat. Biotechnol. 2013, 31, 160-165.
185. Lu, T. K.; Collins, J. J. Engineered bacteriophage targeting gene networks as adjuvants for antibiotic therapy. Proc. Natl. Acad. Sci. USA 2009, 106, 4629-4634.