The emergence of multi-resistant bacterial strains is a major source of concern and has been correlated with the widespread use of antibiotics. The origins of resistance are intensively studied and many mechanisms involved in resistance have been identified, such as exogenous gene acquisition by horizontal gene transfer (HGT), mutations in the targeted functions, and more recently, antibiotic tolerance through persistence. In this review, we focus on factors leading to integron rearrangements and gene capture facilitating antibiotic resistance acquisition, maintenance and spread. The role of stress responses, such as the SOS response, is discussed.
References
[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, doi:10.1046/j.1365-2958.1998.00936.x.
[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, doi:10.1128/JB.187.5.1740-1750.2005.
[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, doi:10.1038/sj.emboj.7600898.
[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, doi:10.1371/journal.pgen.1000793.
[5]
Mazel, D. Integrons: Agents of bacterial evolution. Nat. Rev. Microbiol. 2006, 4, 608–620, doi:10.1038/nrmicro1462.
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, doi:10.1093/jac/42.6.689.
[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, doi:10.1111/j.1365-2958.1989.tb00153.x.
[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, doi:10.1128/JCM.41.8.3542-3547.2003.
[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, doi:10.1093/jac/dkl122.
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, doi:10.1046/j.1365-2958.2002.02861.x.
[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, doi:10.1111/j.1574-6976.2009.00175.x.
[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, doi:10.1126/science.280.5363.605.
[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, doi:10.1128/AEM.00564-12.
[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, doi:10.1128/AAC.06048-11.
[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, doi:10.1099/mic.0.27569-0.
[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, doi:10.1128/JB.00152-08.
[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, doi:10.1111/j.1462-2920.2009.01918.x.
[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, doi:10.1128/AAC.46.7.2162-2168.2002.
[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, doi:10.1128/AAC.48.10.4042-4046.2004.
[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, doi:10.3201/eid1407.080132.
[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, doi:10.1101/gad.1355605.
[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, doi:10.1126/science.1172914.
[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, doi:10.1186/1759-8753-2-6.
[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, doi:10.1371/journal.pgen.1001165.
[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, doi:10.1016/0092-8674(95)90501-4.
[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, doi:10.1128/JB.182.20.5922-5924.2000.
[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, doi:10.1016/j.dnarep.2004.09.008.
[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, doi:10.1111/j.1574-6968.2011.02432.x.
[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 Environmen. 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, doi:10.1128/AAC.6.2.191.
[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, doi:10.1016/j.resmic.2009.11.004.
[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, doi:10.1111/j.1574-6968.2012.02544.x.
[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, doi:10.1073/pnas.1113246109.
[45]
Dubnau, D. DNA uptake in bacteria. Annu. Rev. Microbiol. 1999, 53, 217–244, doi:10.1146/annurev.micro.53.1.217.
[46]
Claverys, J.P.; Martin, B.; Polard, P. The genetic transformation machinery: Composition, localization, and mechanism. FEMS Microbiol. Rev. 2009, 33, 643–656, doi:10.1111/j.1574-6976.2009.00164.x.
[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, doi:10.1111/j.1574-6976.2012.00353.x.
[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.
Lo Scrudato, M.; Blokesch, M. The regulatory network of natural competence and transformation of Vibrio cholerae. PLoS Genet. 2012, 8, e1002778, doi:10.1371/journal.pgen.1002778.
[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, doi:10.1073/pnas.92.8.3616.
[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, doi:10.1016/j.gene.2010.03.003.
[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, doi:10.1093/nar/gkn278.
[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, doi:10.1111/j.1574-6968.2009.01706.x.
[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, doi:10.1016/j.jmb.2005.01.012.
[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, doi:10.1128/JB.00959-08.
[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, doi:10.1371/journal.ppat.1002837.
[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, doi:10.1128/JB.00963-09.
[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, doi:10.1093/nar/gki201.
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, doi:10.1371/journal.pgen.1000786.
[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, doi:10.1128/MMBR.00048-05.
[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, doi:10.1128/AAC.01549-10.
[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, doi:10.1038/nrmicro2382.
[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, doi:10.1371/journal.pgen.1000439.
[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, doi:10.1128/JB.01610-06.
[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, doi:10.1073/pnas.0308052101.
[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, doi:10.1128/JB.185.17.5045-5054.2003.
Garriss, G.; Waldor, M.K.; Burrus, V. Mobile antibiotic resistance encoding elements promote their own diversity. PLoS Genet. 2009, 5, e1000775, doi:10.1371/journal.pgen.1000775.
[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, doi:10.1128/JB.02090-12.
[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, doi:10.1128/JB.183.4.1124-1132.2001.
[80]
Burrus, V.; Waldor, M.K. Formation of SXT tandem arrays and SXT-R391 hybrids. J. Bacteriol. 2004, 186, 2636–2645, doi:10.1128/JB.186.9.2636-2645.2004.
[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, doi:10.1056/NEJM199709043371004.
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, doi:10.1371/journal.pone.0000309.
[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, doi:10.4161/mge.19626.
[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, doi:10.1016/S0378-1097(02)00559-1.
[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, doi:10.1146/annurev.bi.62.070193.003533.
[90]
Stulke, J.; Hillen, W. Carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 1999, 2, 195–201, doi:10.1016/S1369-5274(99)80034-4.
[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, doi:10.1093/nar/gkl734.
[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, doi:10.1038/nrmicro1932.
[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, doi:10.1128/JB.186.11.3516-3524.2004.
[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, doi:10.1099/mic.0.2007/006668-0.
[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, doi:10.1093/nar/gkh908.
[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, doi:10.1007/BF00330320.
[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, doi:10.1073/pnas.94.1.265.
[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, doi:10.1128/JB.186.19.6374-6382.2004.
[101]
Sinha, S.; Cameron, A.D.; Redfield, R.J. Sxy induces a crp-s regulon in Escherichia coli. J. Bacteriol. 2009, 191, 5180–5195, doi:10.1128/JB.00476-09.
[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, doi:10.1128/JB.00671-12.
[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, doi:10.1111/j.1462-2920.2011.02689.x.
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, doi:10.1016/S0895-4356(99)00027-X.
[106]
Haggard, B.E.; Bartsch, L.D. Net changes in antibiotic concentrations downstream from an effluent discharge. J. Environ. Qual. 2009, 38, 343–352, doi:10.2134/jeq2007.0540.
[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, doi:10.1897/09-073.1.
[108]
Kummerer, K. Antibiotics in the aquatic environment—A review—Part I. position="float" 2009, 75, 417–434, doi:10.1016/j. position="float".2008.11.086.
[109]
Kummerer, K. Antibiotics in the aquatic environment—A review—Part II. position="float" 2009, 75, 435–441, doi:10.1016/j. position="float".2008.12.006.
[110]
Hughes, D.; Andersson, D.I. Selection of resistance at lethal and non-lethal antibiotic concentrations. Curr. Opin. Microbiol. 2012, 15, 555–560, doi:10.1016/j.mib.2012.07.005.
[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, doi:10.1016/j.mib.2006.08.006.
[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, doi:10.1128/JB.00791-06.
[115]
Yim, G.; McClure, J.; Surette, M.G.; Davies, J.E. Modulation of Salmonella gene expression by subinhibitory concentrations of quinolones. J. Antibiot. (Tokyo) , 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, doi:10.1016/j.chembiol.2004.07.010.
[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, doi:10.1073/pnas.0608949103.
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, doi:10.1128/AAC.01418-09.
[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, doi:10.1371/journal.pgen.1003144.
[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, doi:10.1111/j.1462-2920.2011.02486.x.
[125]
Gotoh, H.; Kasaraneni, N.; Devineni, N.; Dallo, S.F.; Weitao, T. SOS involvement in stress-inducible biofilm formation. Biofouling 2010, 26, 603–611, doi:10.1080/08927014.2010.501895.
[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, doi:10.1016/S0958-1669(03)00036-3.
[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, doi:10.1093/jac/dks169.
[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, doi:10.1093/mutage/5.1.63.
[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, doi:10.1126/science.1101630.
[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, doi:10.1128/JB.187.4.1515-1518.2005.
[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, doi:10.1159/000069981.
[132]
Mesak, L.R.; Davies, J. Phenotypic changes in ciprofloxacin-resistant Staphylococcus aureus. Res. Microbiol. 2009, 160, 785–791, doi:10.1016/j.resmic.2009.09.013.
[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, doi:10.1128/AAC.01599-07.
[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, doi:10.1128/AAC.00358-09.
[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, doi:10.1128/AAC.50.1.220-225.2006.
[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, doi:10.1128/AAC.01407-10.
[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, doi:10.1016/j.cub.2009.11.039.
[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, doi:10.1371/journal.pgen.1003421.
[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, doi:10.1371/journal.ppat.1002778.
[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, doi:10.1111/j.1574-6976.2007.00082.x.
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, doi:10.1128/JB.188.7.2726-2729.2006.
[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, doi:10.1126/science.1127912.
[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, doi:10.1371/journal.ppat.1002158.
[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, doi:10.1093/jac/dkg427.
[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, doi:10.1128/AAC.01182-10.
[150]
Dorr, T.; Lewis, K.; Vulic, M. SOS response induces persistence to fluoroquinolones in Escherichia coli. PLoS Genet. 2009, 5, e1000760, doi:10.1371/journal.pgen.1000760.
[151]
Dorr, T.; Vulic, M.; Lewis, K. Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli. PLoS Biol. 2010, 8, e1000317, doi:10.1371/journal.pbio.1000317.
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, doi:10.1128/JB.01389-12.
Mcbride, T.J.; Preston, B.D.; Loeb, L.A. Mutagenic spectrum resulting from DNA damage by oxygen radicals. Biochemistry 1991, 30, 207–213, doi:10.1021/bi00215a030.
[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, doi:10.1128/AAC.01495-10.
[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, doi:10.1111/j.1574-6968.2011.02453.x.
[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, doi:10.1016/j.mib.2009.06.018.
[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, doi:10.1111/j.1365-2958.2012.07982.x.
[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, doi:10.1126/science.1211037.
[163]
Shatalin, K.; Shatalina, E.; Mironov, A.; Nudler, E. H2S: A universal defense against antibiotics in bacteria. Science 2011, 334, 986–990, doi:10.1126/science.1209855.
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, doi:10.1016/j.fm.2011.09.014.
[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, doi:10.1128/JB.00412-09.
[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, doi:10.1128/JB.00132-12.
[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, doi:10.1128/MMBR.66.3.373-395.2002.
[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, doi:10.1099/mic.0.026021-0.
[171]
Daly, M.J. A new perspective on radiation resistance based on Deinococcus radiodurans. Nat. Rev. Microbiol. 2009, 7, 237–245, doi:10.1038/nrmicro2073.
[172]
Henle, E.S.; Linn, S. Formation, prevention, and repair of DNA damage by iron/hydrogen peroxid. J. Biol. Chem. 1997, 272, 19095–19098, doi:10.1074/jbc.272.31.19095.
[173]
Keyer, K.; Imlay, J.A. Superoxide accelerates DNA damage by elevating free-iron levels. Proc. Natl. Acad. Sci. USA 1996, 93, 13635–13640, doi:10.1073/pnas.93.24.13635.
[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, doi:10.1128/AAC.00144-08.
[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, doi:10.1371/journal.pgen.1002818.
[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, doi:10.1099/mic.0.042937-0.
[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, doi:10.1007/s00239-010-9352-0.
[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, doi:10.1534/genetics.105.053892.
[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, doi:10.1371/journal.pone.0033514.
[181]
Joelsson, A.; Kan, B.; Zhu, J. Quorum sensing enhances the stress response in Vibrio cholerae. Appl. Environ. Microbiol. 2007, 73, 3742–3746, doi:10.1128/AEM.02804-06.
[182]
Allison, K.R.; Brynildsen, M.P.; Collins, J.J. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 2011, 473, 216–220, doi:10.1038/nature10069.
