20,099
Views
217
CrossRef citations to date
0
Altmetric
Review Article

The impact of insertion sequences on bacterial genome plasticity and adaptability

, ORCID Icon, & ORCID Icon
Pages 709-730 | Received 19 Oct 2016, Accepted 04 Mar 2017, Published online: 13 Apr 2017

References

  • Al-Bayssari C, Valentini C, Gomez C, Reynaud-Gaubert M, Rolain JM. 2015. First detection of insertion sequence element ISPa1328 in the oprD porin gene of an imipenem-resistant Pseudomonas aeruginosa isolate from an idiopathic pulmonary fibrosis patient in Marseille, France. New Microbes New Infect. 7:26–27.
  • Al Bayssari C, Diene SM, Loucif L, Gupta SK, Dabboussi F, Mallat H, Hamze M, Rolain JM. 2014. Emergence of VIM-2 and IMP-15 carbapenemases and inactivation of oprD gene in carbapenem-resistant Pseudomonas aeruginosa clinical isolates from Lebanon. Antimicrob Agents Chemother. 58:4966–4970.
  • Alton NK, Vapnek D. 1979. Nucleotide sequence analysis of the chloramphenicol resistance transposon Tn9. Nature, 282:864–869.
  • Arciola CR, Campoccia D, Gamberini S, Rizzi S, Donati ME, Baldassarri L, Montanaro L. 2004. Search for the insertion element IS256 within the ica locus of Staphylococcus epidermidis clinical isolates collected from biomaterial-associated infections. Biomaterials. 25:4117–25.
  • Arciola CR, Campoccia D, Ravaioli S, Montanaro L. 2015. Polysaccharide intercellular adhesin in biofilm: structural and regulatory aspects. Front Cell Infect Microbiol. 5:7.
  • Aubert D, Naas T, Heritier C, Poirel L, Nordmann P. 2006. Functional characterization of IS1999, an IS4 family element involved in mobilization and expression of beta-lactam resistance genes. J Bacteriol. 188:6506–6514.
  • Aubert D, Naas T, Nordmann P. 2003. IS1999 increases expression of the extended-spectrum beta-lactamase VEB-1 in Pseudomonas aeruginosa. J Bacteriol. 185:5314–5319.
  • Bagge N, Ciofu O, Hentzer M, Campbell JIA, Givskov M, Hoiby N. 2002. Constitutive high expression of chromosomal -lactamase in Pseudomonas aeruginosa caused by a new insertion sequence (IS1669) located in ampD. Antimicrob Agents Chemother. 46:3406–3411.
  • Barany F, Boeke JD, Tomasz A. 1982. Staphylococcal plasmids that replicate and express erythromycin resistance in both Streptococcus pneumoniae and Escherichia coli. Proc Natl Acad Sci. USA, 79:2991–2995.
  • Barker CS, Pruss BM, Matsumura P. 2004. Increased motility of Escherichia coli by insertion sequence element integration into the regulatory region of the flhD operon. J Bacteriol. 186:7529–7537.
  • Bender J, Kleckner N. 1992. Tn10 insertion specificity is strongly dependent upon sequences immediately adjacent to the target-site consensus sequence. Proc Natl Acad Sci USA. 89:7996–8000.
  • Bennett PM. 2004. Genome plasticity. In: Genomics, proteomics, and clinical bacteriology. Totowa (NJ): Humana Press; p. 71–113.
  • Bennett PM. 2008. Plasmid encoded antibiotic resistance: acquisition and transfer of antibiotic resistance genes in bacteria. Br J Pharmacol. 153 Suppl 1:S347–S357.
  • Benson MA, Ohneck EA, Ryan C, Alonzo F, 3rd, Smith H, Narechania A, Kolokotronis SO, Satola SW, Uhlemann AC, Sebra R, et al. 2014. Evolution of hypervirulence by a MRSA clone through acquisition of a transposable element. Mol Microbiol. 93:664–681.
  • Beuzon CR, Chessa D, Casadesus J. 2004. IS200: an old and still bacterial transposon. Int Microbiol. 7:3–12.
  • Beuzon CR, Marques S, Casadesus J. 1999. Repression of IS200 transposase synthesis by RNA secondary structures. Nucleic Acids Res. 27:3690–3695.
  • Bichsel M, Barbour AD, Wagner A. 2013. Estimating the fitness effect of an insertion sequence. J Math Biol. 66:95–114.
  • Blot M. 1994. Transposable elements and adaptation of host bacteria. Genetica 93:5–12.
  • Blount ZD, Barrick JE, Davidson CJ, Lenski RE. 2012. Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature. 489:513–518.
  • Bohn C, Bouloc P. 1998. The Escherichia coli cmlA gene encodes the multidrug efflux pump Cmr/MdfA and is responsible for isopropyl-beta-d-thiogalactopyranoside exclusion and spectinomycin sensitivity. J Bacteriol. 180:6072–6075.
  • Bolognese F, Di Lecce C, Galli E, Barbieri P. 1999. Activation and inactivation of Pseudomonas stutzeri methylbenzene catabolism pathways mediated by a transposable element. Appl Environ Microbiol. 65:1876–1882.
  • Bongers RS, Hoefnagel MH, Starrenburg MJ, Siemerink MA, Arends JG, Hugenholtz J, Kleerebezem M. 2003. IS981-mediated adaptive evolution recovers lactate production by ldhB transcription activation in a lactate dehydrogenase-deficient strain of Lactococcus lactis. J Bacteriol. 185:4499–4507.
  • Boutoille D, Corvec S, Caroff N, Giraudeau C, Espaze E, Caillon J, Plésiat P, Reynaud A. 2004. Detection of an IS21 insertion sequence in the mexR gene of Pseudomonas aeruginosa increasing β-lactam resistance. FEMS Microbiol Lett. 230:143–6.
  • Brau B, Pilz U, Piepersberg W. 1984a. Genes for gentamicin-(3)-N-acetyltransferases III and IV: I. Nucleotide sequence of the AAC(3)-IV gene and possible involvement of an IS140 element in its expression. MGG Mol. General Genet. 193:179–187.
  • Brau B, Pilz U, Piepersberg W. 1984b. Genes for gentamicin-(3)-N-acetyltransferases III and IV: I. Nucleotide sequence of the AAC(3)-IV gene and possible involvement of an IS140 element in its expression. Mol Gen Genet. 193:179–187.
  • Cabrejos ME, Zhao HL, Guacucano M, Bueno S, Levican G, Garcia E, Jedlicki E, Holmes DS. 1999. IST1 insertional inactivation of the resB gene: implications for phenotypic switching in Thiobacillus ferrooxidans. FEMS Microbiol Lett. 175:223–229.
  • Cannatelli A, Giani T, D'Andrea MM, Di Pilato V, Arena F, Conte V, Tryfinopoulou K, Vatopoulos A, Rossolini GM, Group CS. 2014. MgrB inactivation is a common mechanism of colistin resistance in KPC-producing Klebsiella pneumoniae of clinical origin. Antimicrob Agents Chemother. 58:5696–5703.
  • Cao V, Lambert T, Courvalin P. 2002. ColE1-like plasmid pIP843 of Klebsiella pneumoniae encoding extended-spectrum beta-lactamase CTX-M-17. Antimicrob Agents Chemother. 46:1212–1217.
  • Carlson PE, Jr., Horzempa J, O'Dee DM, Robinson CM, Neophytou P, Labrinidis A, Nau GJ. 2009. Global transcriptional response to spermine, a component of the intramacrophage environment, reveals regulation of Francisella gene expression through insertion sequence elements. J Bacteriol. 191:6855–6864.
  • Cattoir V, Nordmann P, Silva-Sanchez J, Espinal P, Poirel L. 2008. ISEcp1-mediated transposition of qnrB-like gene in Escherichia coli. Antimicrob Agents Chemother. 52:2929–2932.
  • Chain PS, Carniel E, Larimer FW, Lamerdin J, Stoutland PO, Regala WM, Georgescu AM, Vergez LM, Land ML, Motin VL, et al. 2004. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis. Proc Natl Acad Sci USA. 101:13826–13831.
  • Chandler M, Mahillon J. 2002. Insertion Sequences Revisited. In: Mobile DNA II. Washington (DC): ASM Press.
  • Charlier D, Piette J, Glansdorff N. 1982. IS3 can function as a mobile promoter in E. coli. Nucleic Acids Res. 10:5935–5948.
  • Chen TL, Wu RC, Shaio MF, Fung CP, Cho WL. 2008a. Acquisition of a plasmid-borne blaOXA-58 gene with an upstream IS1008 insertion conferring a high level of carbapenem resistance to Acinetobacter baumannii. Antimicrob Agents Chemother. 52:2573–2580.
  • Chen YG, Zhang Y, Yu YS, Qu TT, Wei ZQ, Shen P, Li LJ. 2008b. In vivo development of carbapenem resistance in clinical isolates of Enterobacter aerogenes producing multiple beta-lactamases. Int J Antimicrob Agents 32:302–307.
  • Christie-Oleza JA, Lanfranconi MP, Nogales B, Lalucat J, Bosch R. 2009. Conjugative interaction induces transposition of ISPst9 in Pseudomonas stutzeri AN10. J Bacteriol. 191:1239–1247.
  • Christie-Oleza JA, Nogales B, Martin-Cardona C, Lanfranconi MP, Alberti S, Lalucat J, Bosch R. 2008. ISPst9, an ISL3-like insertion sequence from Pseudomonas stutzeri AN10 involved in catabolic gene inactivation. Int Microbiol. 11:101–110.
  • Claus H, Borrow R, Achtman M, Morelli G, Kantelberg C, Longworth E, Frosch M, Vogel U. 2003. Genetics of capsule O-acetylation in serogroup C, W-135 and Y meningococci. Mol Microbiol. 51:227–239.
  • Clough SJ, Flavier AB, Schell MA, Denny TP. 1997. Differential Expression of Virulence Genes and Motility in Ralstonia (Pseudomonas) solanacearum during Exponential Growth. Appl Environ Microbiol. 63:844–850.
  • Cluzel PJ, Chopin A, Ehrlich SD, Chopin MC. 1991. Phage abortive infection mechanism from Lactococcus Lactis Subsp lactis, expression of which is mediated by an Iso-ISS1 element. Appl Environ Microbiol. 57:3547–3551.
  • Cole ST, Eiglmeier K, Parkhill J, James KD, Thomson NR, Wheeler PR, Honore N, Garnier T, Churcher C, Harris D, et al. 2001. Massive gene decay in the leprosy bacillus. Nature. 409:1007–1011.
  • Coleman NV, Richardson-Harris J, Wilson NL, Holmes AJ. 2014. Insertion sequence ISPst4 activates pUC plasmid replication in Pseudomonas stutzeri. FEMS Microbiol Lett. 356:242–249.
  • Collard JM, Provoost A, Taghavi S, Mergeay M. 1993. A new type of Alcaligenes eutrophus CH34 zinc resistance generated by mutations affecting regulation of the cnr cobalt-nickel resistance system. J Bacteriol. 175:779–784.
  • Conlon KM, Humphreys H, O'Gara JP. 2004. Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. J Bacteriol. 186:6208–6219.
  • Cooper VS, Schneider D, Blot M, Lenski RE. 2001. Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J Bacteriol. 183:2834–2841.
  • Coros AM, Twiss E, Tavakoli NP, Derbyshire KM. 2005. Genetic Evidence that GTP Is Required for Transposition of IS903 and Tn552 in Escherichia coli. J Bacteriol. 187:4598–4606.
  • Corvec S, Caroff N, Espaze E, Giraudeau C, Drugeon H, Reynaud A. 2003. AmpC cephalosporinase hyperproduction in Acinetobacter baumannii clinical strains. J Antimicrob Chemother. 52:629–635.
  • Coucheron DH. 1991. An Acetobacter xylinum insertion sequence element associated with inactivation of cellulose production. J Bacteriol. 173:5723–5731.
  • Couto I, Wu SW, Tomasz A, de Lencastre H. 2003. Development of methicillin resistance in clinical isolates of Staphylococcus sciuri by transcriptional activation of the mecA homologue native to species. J Bacteriol. 185:645–653.
  • Craig NL. 1997. Target site selection in transposition. Annu Rev Biochem. 66:437–474.
  • Craig NL, Craigie R, Gellert M, Lambowitz AM. 2002. Mobile DNA II. Washington, DC: American Society of Microbiology.
  • Curcio MJ, Derbyshire KM. 2003. The outs and ins of transposition: from mu to kangaroo. Nat Rev Mol Cell Biol. 4:865–877.
  • Dalrymple B. 1987. Novel rearrangements of IS30 carrying plasmids leading to the reactivation of gene expression. Mol Gen Genet. 207:413–420.
  • Dalrymple B, Arber W. 1985. Promotion of RNA transcription on the insertion element IS30 of E. coli K12. EMBO J. 4:2687–2693.
  • De Palmenaer D, Siguier P, Mahillon J. 2008. IS4 family goes genomic. BMC Evol Biol. 8:18.
  • Derbyshire KM, Kramer M, Grindley ND. 1990. Role of instability in the cis action of the insertion sequence IS903 transposase. Proc Natl Acad Sci USA. 87:4048–4052.
  • DeShazer D, Wood GE, Friedman RL. 1994. Molecular characterization of catalase from Bordetella pertussis: identification of the katA promoter in an upstream insertion sequence. Mol Microbiol. 14:123–130.
  • Di Lorenzo M, Stork M, Tolmasky ME, Actis LA, Farrell D, Welch TJ, Crosa LM, Wertheimer AM, Chen Q, Salinas P, et al. 2003. Complete sequence of virulence plasmid pJM1 from the marine fish pathogen Vibrio anguillarum strain 775. J Bacteriol. 185:5822–5830.
  • Diene SM, L'Homme T, Bellulo S, Stremler N, Dubus JC, Mely L, Leroy S, Degand N, Rolain JM. 2013. ISPa46, a novel insertion sequence in the oprD porin gene of an imipenem-resistant Pseudomonas aeruginosa isolate from a cystic fibrosis patient in Marseille, France. Int J Antimicrob Agents. 42:268–271.
  • Doolittle WF, Sapienza C. 1980. Selfish genes, the phenotype paradigm and genome evolution. Nature. 284:601–603.
  • Drevinek P, Baldwin A, Lindenburg L, Joshi LT, Marchbank A, Vosahlikova S, Dowson CG, Mahenthiralingam E. 2010. Oxidative stress of Burkholderia cenocepacia induces insertion sequence-mediated genomic rearrangements that interfere with macrorestriction-based genotyping. J Clin Microbiol. 48:34–40.
  • Eichenbaum Z, Livneh Z. 1998. UV light induces IS10 transposition in Escherichia coli. Genetics. 149:1173–1181.
  • Ellis MJ, Trussler RS, Haniford DB. 2015a. A cis-encoded sRNA, Hfq and mRNA secondary structure act independently to suppress IS200 transposition. Nucleic Acids Res. 43:6511–6527.
  • Ellis MJ, Trussler RS, Haniford DB. 2015b. Hfq binds directly to the ribosome-binding site of IS10 transposase mRNA to inhibit translation. Mol Microbiol. 96:633–650.
  • Escoubas JM, Prere MF, Fayet O, Salvignol I, Galas D, Zerbib D, Chandler M. 1991. Translational control of transposition activity of the bacterial insertion sequence IS1. EMBO J. 10:705–712.
  • Evans JC, Segal H. 2007. A novel insertion sequence, ISPa26, in oprD of Pseudomonas aeruginosa is associated with carbapenem resistance. Antimicrob Agents Chemother. 51:3776–3777.
  • Fahrner KA, Berg HC. 2015. Mutations that stimulate flhDC expression in Escherichia coli. J Bacteriol. 197:3087–3096.
  • Ferenci T. 2003. What is driving the acquisition of mutS and rpoS polymorphisms in Escherichia coli? Trends Microbiol. 11:457–461.
  • Fowler RC, Hanson ND. 2014. Emergence of carbapenem resistance due to the novel insertion sequence ISPa8 in Pseudomonas aeruginosa. PLoS One. 9:e91299.
  • Fujimura T, Murakami K. 2008. Staphylococcus aureus clinical isolate with high-level methicillin resistance with an lytH mutation caused by IS1182 insertion. Antimicrob Agents Chemother. 52:643–647.
  • Furi L, Haigh R, Al Jabri ZJ, Morrissey I, Ou HY, Leon-Sampedro R, Martinez JL, Coque TM, Oggioni MR. 2016. Dissemination of novel antimicrobial resistance mechanisms through the insertion sequence mediated spread of metabolic genes. Front Microbiol. 7:1008.
  • Gaffe J, McKenzie C, Maharjan RP, Coursange E, Ferenci T, Schneider D. 2011. Insertion sequence-driven evolution of Escherichia coli in chemostats. J Mol Evol. 72:398–412.
  • Garnier F, Janapatla RP, Charpentier E, Masson G, Grelaud C, Stach JF, Denis F, Ploy MC. 2007. Insertion sequence 1515 in the ply gene of a type 1 clinical isolate of Streptococcus pneumoniae abolishes pneumolysin expression. J Clin Microbiol. 45:2296–2297.
  • Gerischer U, D'Argenio DA, Ornston LN. 1996. IS1236, a newly discovered member of the IS3 family, exhibits varied patterns of insertion into the Acinetobacter calcoaceticus chromosome. Microbiology. 142:1825–1831.
  • Ghanekar K, McBride A, Dellagostin O, Thorne S, Mooney R, McFadden J. 1999. Stimulation of transposition of the Mycobacterium tuberculosis insertion sequence IS6110 by exposure to a microaerobic environment. Mol Microbiol. 33:982–993.
  • Glansdorff N, Charlier D, Zafarullah M. 1981. Activation of gene expression by IS2 and IS3. Cold Spring Harb Symp Quant Biol. 45 Pt 1:153–156.
  • Godoy VG, Fox MS. 2000. Transposon stability and a role for conjugational transfer in adaptive mutability. Proc Natl Acad Sci USA. 97:7393–7398.
  • Goussard S, Sougakoff W, Mabilat C, Bauernfeind A, Courvalin P. 1991. An IS1-like element is responsible for high-level synthesis of extended-spectrum beta-lactamase TEM-6 in Enterobacteriaceae. J Gen Microbiol. 137:2681–2687.
  • Grass G, Grosse C, Nies DH. 2000. Regulation of the cnr cobalt and nickel resistance determinant from Ralstonia sp. strain CH34. J Bacteriol. 182:1390–1398.
  • Graves JL, Jr., Tajkarimi M, Cunningham Q, Campbell A, Nonga H, Harrison SH, Barrick JE. 2015. Rapid evolution of silver nanoparticle resistance in Escherichia coli. Front Genet. 6:42.
  • Gregory ST, Dahlberg AE. 2008. Transposition of an insertion sequence, ISTth7, in the genome of the extreme thermophile Thermus thermophilus HB8. FEMS Microbiol Lett. 289:187–192.
  • Gueguen E, Rousseau P, Duval-Valentin G, Chandler M. 2006. Truncated forms of IS911 transposase downregulate transposition. Mol Microbiol. 62:1102–1116.
  • Haggoud A, Reysset G, Azeddoug H, Sebald M. 1994. Nucleotide sequence analysis of two 5-nitroimidazole resistance determinants from Bacteroides strains and of a new insertion sequence upstream of the two genes. Antimicrob Agents Chemother. 38:1047–1051.
  • Hallet B, Rezsohazy R, Mahillon J, Delcour J. 1994. IS231A insertion specificity: consensus sequence and DNA bending at the target site. Mol Microbiol. 14:131–139.
  • Hammerschmidt S, Hilse R, van Putten JP, Gerardy-Schahn R, Unkmeir A, Frosch M. 1996. Modulation of cell surface sialic acid expression in Neisseria meningitidis via a transposable genetic element. EMBO J. 15:192–198.
  • Han HJ, Kuwae A, Abe A, Arakawa Y, Kamachi K. 2011. Differential expression of type III effector BteA protein due to IS481 insertion in Bordetella pertussis. PLoS One. 6:e17797.
  • Haniford DB, Ellis MJ. 2015. Transposons Tn10 and Tn5. Microbiol Spectr. 3:MDNA3.
  • Haren L, Betermier M, Polard P, Chandler M. 1997. IS911-mediated intramolecular transposition is naturally temperature sensitive. Mol Microbiol. 25:531–540.
  • He T, Nishihara T, Demuth DR, Ishikawa I. 1999. A novel insertion sequence increases the expression of leukotoxicity in Actinobacillus actinomycetemcomitans clinical isolates. J Periodontol. 70:1261–1268.
  • Heritier C, Poirel L, Nordmann P. 2006. Cephalosporinase over-expression resulting from insertion of ISAba1 in Acinetobacter baumannii. Clin Microbiol Infect. 12:123–130.
  • Hernandez-Alles S, Benedi VJ, Martinez-Martinez L, Pascual A, Aguilar A, Tomas JM, Alberti S. 1999. Development of resistance during antimicrobial therapy caused by insertion sequence interruption of porin genes. Antimicrob Agents Chemother. 43:937–939.
  • Hinton DM, Musso RE. 1983. Specific in vitro transcription of the insertion sequence IS2. J Mol Biol. 169:53–81.
  • Hu ST, Hwang JH, Lee LC, Lee CH, Li PL, Hsieh YC. 1994. Functional analysis of the 14 kDa protein of insertion sequence 2. J Mol Biol. 236:503–513.
  • Hu WY, Derbyshire KM. 1998. Target choice and orientation preference of the insertion sequence IS903. J Bacteriol. 180:3039–3048.
  • Hubner A, Hendrickson W. 1997. A fusion promoter created by a new insertion sequence, IS1490, activates transcription of 2,4,5-trichlorophenoxyacetic acid catabolic genes in Burkholderia cepacia AC1100. J Bacteriol. 179:2717–2723.
  • Hubner P, Iida S, Arber W. 1987. A transcriptional terminator sequence in the prokaryotic transposable element IS1. Mol Gen Genet. 206:485–490.
  • Iranzo J, Gomez MJ, Lopez de Saro FJ, Manrubia S. 2014. Large-scale genomic analysis suggests a neutral punctuated dynamics of transposable elements in bacterial genomes. PLoS Comput Biol. 10:e1003680.
  • Jaurin B, Normark S. 1983. Insertion of IS2 creates a novel ampC promoter in Escherichia coli. Cell 32:809–816.
  • Jayol A, Poirel L, Villegas MV, Nordmann P. 2015. Modulation of mgrB gene expression as a source of colistin resistance in Klebsiella oxytoca. Int J Antimicrob Agents. 46:108–110.
  • Jellen-Ritter AS, Kern WV. 2001. Enhanced expression of the multidrug efflux pumps AcrAB and AcrEF associated with insertion element transposition in Escherichia coli mutants selected with a fluoroquinolone. Antimicrob Agents Chemother. 45:1467–1472.
  • Jeong EL, Timmis JN. 2000. Novel insertion sequence elements associated with genetic heterogeneity and phenotype conversion in Ralstonia solanacearum. J Bacteriol. 182:4673–4676.
  • Jones LA, McIver CJ, Kim MJ, Rawlinson WD, White PA. 2005. The aadB gene cassette is associated with blaSHV genes in Klebsiella species producing extended-spectrum beta-lactamases. Antimicrob Agents Chemother. 49:794–797.
  • Kalantar-Neyestanaki D, Emaneini M, Jabalameli F, Taherikalani M, Mirsalehian A. 2015. ISPpu22, a novel insertion sequence in the oprD porin gene of a carbapenem-resistant Pseudomonas aeruginosa isolate from a burn patient in Tehran, Iran. Iran J Microbiol. 7:247–250.
  • Kallastu A, Horak R, Kivisaar M. 1998. Identification and characterization of IS1411, a new insertion sequence which causes transcriptional activation of the phenol degradation genes in Pseudomonas putida. J Bacteriol. 180:5306–5312.
  • Kamruzzaman M, Patterson JD, Shoma S, Ginn AN, Partridge SR, Iredell JR. 2015. Relative strengths of promoters provided by common mobile genetic elements associated with resistance gene expression in Gram-negative bacteria. Antimicrob Agents Chemother. 59:5088–5091.
  • Karim A, Poirel L, Nagarajan S, Nordmann P. 2001. Plasmid-mediated extended-spectrum beta-lactamase (CTX-M-3 like) from India and gene association with insertion sequence ISEcp1. FEMS Microbiol Lett. 201:237–241.
  • Kato N, Yamazoe K, Han CG, Ohtsubo E. 2003. New insertion sequence elements in the upstream region of cfiA in imipenem-resistant Bacteroides fragilis strains. Antimicrob Agents Chemother. 47:979–985.
  • Kiem S, Oh WS, Peck KR, Lee NY, Lee J-Y, Song J-H, Hwang ES, Kim E-C, Cha CY, Choe K-W. 2004. Phase variation of biofilm formation in Staphylococcus aureus by IS256 insertion and its impact on the capacity adhering to polyurethane surface. J Korean Med Sci. 19:779–782.
  • Kiss J, Nagy Z, Toth G, Kiss GB, Jakab J, Chandler M, Olasz F. 2007. Transposition and target specificity of the typical IS30 family element IS1655 from Neisseria meningitidis. Mol Microbiol. 63:1731–1747.
  • Kleckner N, Chalmers RM, Kwon D, Sakai J, Bolland S. 1996. Tn10 and IS10 transposition and chromosome rearrangements: Mechanism and regulation in vivo and in vitro. In: Transposable Elements. p. 49–82.
  • Kobayashi K, Tsukagoshi N, Aono R. 2001. Suppression of hypersensitivity of Escherichia coli acrB mutant to organic solvents by integrational activation of the acrEF operon with the IS1 or IS2 element. J Bacteriol. 183:2646–2653.
  • Lapierre L, Mollet B, Germond JE. 2002. Regulation and adaptive evolution of lactose operon expression in Lactobacillus delbrueckii. J Bacteriol. 184:928–935.
  • Lartigue MF, Poirel L, Aubert D, Nordmann P. 2006. In vitro analysis of ISEcp1B-mediated mobilization of naturally occurring beta-lactamase gene blaCTX-M of Kluyvera ascorbata. Antimicrob Agents Chemother. 50:1282–1286.
  • Lartigue MF, Poirel L, Nordmann P. 2004. Diversity of genetic environment of bla(CTX-M) genes. FEMS Microbiol Lett. 234:201–207.
  • Lee CH, Chu C, Liu JW, Chen YS, Chiu CJ, Su LH. 2007. Collateral damage of flomoxef therapy: in vivo development of porin deficiency and acquisition of blaDHA-1 leading to ertapenem resistance in a clinical isolate of Klebsiella pneumoniae producing CTX-M-3 and SHV-5 beta-lactamases. J Antimicrob Chemother. 60:410–413.
  • Lee KY, Hopkins JD, Syvanen M. 1990. Direct involvement of IS26 in an antibiotic resistance operon. J Bacteriol. 172:3229–3236.
  • Leelaporn A, Firth N, Byrne ME, Roper E, Skurray RA. 1994. Possible role of insertion sequence IS257 in dissemination and expression of high- and low-level trimethoprim resistance in staphylococci. Antimicrob Agents Chemother. 38:2238–2244.
  • Lessie TG, Wood MS, Byrne A, Ferrante A. 1990. Transposable gene-activating elements in Pseudomonas cepacia. In: Pseudomonas: biotransformations, pathogenesis, and evolving biotechnology. Washington (DC): American Society for Microbiology; p. 279–291.
  • Lewis JP, Macrina FL. 1998. IS195, an insertion sequence-like element associated with protease genes in Porphyromonas gingivalis. Infect Immunun. 66:3035–3042.
  • Lipton MS, Pasa-Tolic L, Anderson GA, Anderson DJ, Auberry DL, Battista JR, Daly MJ, Fredrickson J, Hixson KK, Kostandarithes H, et al. 2002. Global analysis of the Deinococcus radiodurans proteome by using accurate mass tags. Proc Natl Acad Sci USA. 99:11049–11054.
  • Lopez de Felipe F, Magni C, de Mendoza D, Lopez P. 1996. Transcriptional activation of the citrate permease P gene of Lactococcus lactis biovar diacetylactis by an insertion sequence-like element present in plasmid pCIT264. Mol Gen Genet. 250:428–436.
  • Luque I, Andujar A, Jia L, Zabulon G, de Marsac NT, Flores E, Houmard J. 2006. Regulated expression of glutamyl-tRNA synthetase is directed by a mobile genetic element in the cyanobacterium Tolypothrix sp. PCC 7601. Mol Microbiol. 60:1276–1288.
  • Machida Y, Machida C, Ohtsubo E. 1982. A novel type of transposon generated by insertion element IS102 present in a pSC101 derivative. Cell. 30:29–36.
  • Mahillon J, Chandler M. 1998. Insertion sequences. Microbiol Mol Biol Rev. 62:725–774.
  • Maki H, McCallum N, Bischoff M, Wada A, Berger-Bachi B. 2004. tcaA inactivation increases glycopeptide resistance in Staphylococcus aureus. Antimicrob Agents Chemother. 48:1953–1959.
  • Maki H, Murakami K. 1997. Formation of potent hybrid promoters of the mutant llm gene by IS256 transposition in methicillin-resistant Staphylococcus aureus. J Bacteriol. 179:6944–6948.
  • Mennecier S, Servant P, Coste G, Bailone A, Sommer S. 2006. Mutagenesis via IS transposition in Deinococcus radiodurans. Mol Microbiol. 59:317–325.
  • Mitchell C, Gao L, Demuth DR. 2003. Positive and negative cis-acting regulatory sequences control expression of leukotoxin in Actinobacillus actinomycetemcomitans 652. Infect Immunun. 71:5640–5649.
  • Moffatt JH, Harper M, Adler B, Nation RL, Li J, Boyce JD. 2011. Insertion sequence ISAba11 is involved in colistin resistance and loss of lipopolysaccharide in Acinetobacter baumannii. Antimicrob Agents Chemother. 55:3022–3024.
  • Mosharrafa E, Pilacinski W, Zissler J, Fiandt M, Szybalski W. 1976. Insertion sequence IS2 near the gene for prophage lambda excision. Mol Gen Genet. 147:103–109.
  • Mussi MA, Limansky AS, Viale AM. 2005. Acquisition of resistance to carbapenems in multidrug-resistant clinical strains of Acinetobacter baumannii: natural insertional inactivation of a gene encoding a member of a novel family of beta-barrel outer membrane proteins. Antimicrob Agents Chemother. 49:1432–1440.
  • Naas T, Cuzon G, Truong HV, Nordmann P. 2012. Role of ISKpn7 and deletions in blaKPC gene expression. Antimicrob Agents Chemother. 56:4753–4759.
  • Naas T, Philippon L, Poirel L, Ronco E, Nordmann P. 1999. An SHV-derived extended-spectrum beta-lactamase in Pseudomonas aeruginosa. Antimicrob Agents Chemother. 43:1281–1284.
  • Nagai T, Tran LS, Inatsu Y, Itoh Y. 2000. A new IS4 family insertion sequence, IS4Bsu1, responsible for genetic instability of poly-gamma-glutamic acid production in Bacillus subtilis. J Bacteriol. 182:2387–2392.
  • Nagy Z, Chandler M. 2004. Regulation of transposition in bacteria. Res Microbiol. 155:387–398.
  • Naville M, Gautheret D. 2010. Premature terminator analysis sheds light on a hidden world of bacterial transcriptional attenuation. Genome Biol. 11:R97.
  • Nevers P, Saedler H. 1977. Transposable genetic elements as agents of gene instability and chromosomal rearrangements. Nature. 268:109–115.
  • Newcombe J, Cartwright K, Dyer S, McFadden J. 1998. Naturally occurring insertional inactivation of the porA gene of Neisseria meningitidis by integration of IS1301. Mol Microbiol. 30:453–454.
  • Nordmann P, Lartigue MF, Poirel L. 2008. Beta-lactam induction of ISEcp1B-mediated mobilization of the naturally occurring bla(CTX-M) beta-lactamase gene of Kluyvera ascorbata. FEMS Microbiol Lett. 288:247–249.
  • Ohtsubo Y, Genka H, Komatsu H, Nagata Y, Tsuda M. 2005. High-temperature-induced transposition of insertion elements in Burkholderia multivorans ATCC 17616. Appl Environ Microbiol. 71:1822–1828.
  • Olasz F, Kiss J, Konig P, Buzas Z, Stalder R, Arber W. 1998. Target specificity of insertion element IS30. Mol Microbiol. 28:691–704.
  • Olliver A, Valle M, Chaslus-Dancla E, Cloeckaert A. 2005. Overexpression of the multidrug efflux operon acrEF by insertional activation with IS1 or IS10 elements in Salmonella enterica serovar Typhimurium DT204 acrB mutants selected with fluoroquinolones. Antimicrob Agents Chemother. 49:289–301.
  • Papadopoulos D, Schneider D, Meier-Eiss J, Arber W, Lenski RE, Blot M. 1999. Genomic evolution during a 10,000-generation experiment with bacteria. Proc Natl Acad Sci USA. 96:3807–3812.
  • Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, Holden MT, Churcher CM, Bentley SD, Mungall KL, et al. 2003. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet. 35:32–40.
  • Pasternak C, Ton-Hoang B, Coste G, Bailone A, Chandler M, Sommer S. 2010. Irradiation-induced Deinococcus radiodurans genome fragmentation triggers transposition of a single resident insertion sequence. PLoS Genet. 6:e1000799.
  • Perez M, Calles-Enriquez M, del Rio B, Ladero V, Martin MC, Fernandez M, Alvarez MA. 2015. IS256 abolishes gelatinase activity and biofilm formation in a mutant of the nosocomial pathogen Enterococcus faecalis V583. Can J Microbiol. 61:517–519.
  • Petersen C, Moller LB, Valentin-Hansen P. 2002. The cryptic adenine deaminase gene of Escherichia coli. Silencing by the nucleoid-associated DNA-binding protein, H-NS, and activation by insertion elements. J Biol Chem. 277:31373–31380.
  • Pilacinski W, Mosharrafa E, Edmundson R, Zissler J, Fiandt M, Szybalski W. 1977. Insertion sequence IS2 associated with int-constitutive mutants of bacteriophage lambda. Gene. 2:61–74.
  • Podglajen I, Breuil J, Casin I, Collatz E. 1995. Genotypic identification of two groups within the species Bacteroides fragilis by ribotyping and by analysis of PCR-generated fragment patterns and insertion sequence content. J Bacteriol. 177:5270–5275.
  • Podglajen I, Breuil J, Collatz E. 1994. Insertion of a novel DNA sequence, 1S1186, upstream of the silent carbapenemase gene cfiA, promotes expression of carbapenem resistance in clinical isolates of Bacteroides fragilis. Mol Microbiol. 12:105–114.
  • Podglajen I, Breuil J, Rohaut A, Monsempes C, Collatz E. 2001. Multiple mobile promoter regions for the rare carbapenem resistance gene of Bacteroides fragilis. J Bacteriol. 183:3531–3535.
  • Poirel L, Cabanne L, Vahaboglu H, Nordmann P. 2005a. Genetic environment and expression of the extended-spectrum beta-lactamase blaPER-1 gene in Gram-negative bacteria. Antimicrob Agents Chemother. 49:1708–1713.
  • Poirel L, Decousser JW, Nordmann P. 2003. Insertion sequence ISEcp1B is involved in expression and mobilization of a bla(CTX-M) beta-lactamase gene. Antimicrob Agents Chemother. 47:2938–2945.
  • Poirel L, Jayol A, Bontron S, Villegas MV, Ozdamar M, Turkoglu S, Nordmann P. 2015. The mgrB gene as a key target for acquired resistance to colistin in Klebsiella pneumoniae. J Antimicrob Chemother. 70:75–80.
  • Poirel L, Lartigue MF, Decousser JW, Nordmann P. 2005b. ISEcp1B-mediated transposition of blaCTX-M in Escherichia coli. Antimicrob Agents Chemother. 49:447–450.
  • Poirel L, Marque S, Heritier C, Segonds C, Chabanon G, Nordmann P. 2005c. OXA-58, a novel class D {beta}-lactamase involved in resistance to carbapenems in Acinetobacter baumannii. Antimicrob Agents Chemother. 49:202–208.
  • Polard P, Seroude L, Fayet O, Prere MF, Chandler M. 1994. One-ended insertion of IS911. J Bacteriol. 176:1192–1196.
  • Prentki P, Teter B, Chandler M, Galas DJ. 1986. Functional promoters created by the insertion of transposable element IS1. J Mol Biol. 191:383–393.
  • Prere MF, Chandler M, Fayet O. 1990. Transposition in Shigella dysenteriae: isolation and analysis of IS911, a new member of the IS3 group of insertion sequences. J Bacteriol. 172:4090–4099.
  • Preston A, Parkhill J, Maskell DJ. 2004. The bordetellae: lessons from genomics. Nat Rev Microbiol. 2:379–390.
  • Prudhomme M, Turlan C, Claverys JP, Chandler M. 2002. Diversity of Tn4001 transposition products: the flanking IS256 elements can form tandem dimers and IS circles. J Bacteriol. 184:433–443.
  • Rajeshwari R, Sonti RV. 2000. Stationary-phase variation due to transposition of novel insertion elements in Xanthomonas oryzae pv. oryzae. J Bacteriol. 182:4797–4802.
  • Randall CP, Gupta A, Jackson N, Busse D, O'Neill AJ. 2015. Silver resistance in Gram-negative bacteria: a dissection of endogenous and exogenous mechanisms. J Antimicrob Chemother. 70:1037–1046.
  • Rasmussen BA, Kovacs E. 1991. Identification and DNA sequence of a new Bacteroides fragilis insertion sequence-like element. Plasmid. 25:141–144.
  • Reynolds AE, Felton J, Wright A. 1981. Insertion of DNA activates the cryptic bgl operon in E. coli K12. Nature. 293:625–629.
  • Rezwan F, Lan R, Reeves PR. 2004. Molecular basis of the indole-negative reaction in Shigella strains: extensive damages to the tna operon by insertion sequences. J Bacteriol. 186:7460–7465.
  • Roberts D, Hoopes BC, McClure WR, Kleckner N. 1985. IS10 transposition is regulated by DNA adenine methylation. Cell 43:117–130.
  • Rogers MB, Bennett TK, Payne CM, Smith CJ. 1994. Insertional activation of cepA leads to high-level beta-lactamase expression in Bacteroides fragilis clinical isolates. J Bacteriol. 176:4376–4384.
  • Rohmer L, Fong C, Abmayr S, Wasnick M, Larson Freeman TJ, Radey M, Guina T, Svensson K, Hayden HS, Jacobs M, et al. 2007. Comparison of Francisella tularensis genomes reveals evolutionary events associated with the emergence of human pathogenic strains. Genome Biol. 8:R102.
  • Rojo-Bezares B, Estepa V, Cebollada R, de Toro M, Somalo S, Seral C, Castillo FJ, Torres C, Saenz Y. 2014. Carbapenem-resistant Pseudomonas aeruginosa strains from a Spanish hospital: characterization of metallo-beta-lactamases, porin OprD and integrons. Int J Med Microbiol. 304:405–414.
  • Ross JA, Wardle SJ, Haniford DB. 2010. Tn10/IS10 transposition is downregulated at the level of transposase expression by the RNA-binding protein Hfq. Mol Microbiol. 78:607–621.
  • Rudant E, Courvalin P, Lambert T. 1998. Characterization of IS18, an element capable of activating the silent aac(6')-Ij gene of Acinetobacter sp. 13 strain BM2716 by transposition. Antimicrob Agents Chemother. 42:2759–2761.
  • Ruiz-Martinez L, Lopez-Jimenez L, d'Ostuni V, Fuste E, Vinuesa T, Vinas M. 2011. A mechanism of carbapenem resistance due to a new insertion element (ISPa133) in Pseudomonas aeruginosa. Int Microbiol. 14:51–58.
  • Saedler H, Reif HJ, Hu S, Davidson N. 1974. IS2, a genetic element for turn-off and turn-on of gene activity in E. coli. Mol Gen Genet. 132:265–289.
  • Safi H, Barnes PF, Lakey DL, Shams H, Samten B, Vankayalapati R, Howard ST. 2004. IS6110 functions as a mobile, monocyte-activated promoter in Mycobacterium tuberculosis. Mol Microbiol. 52:999–1012.
  • Schaeffer LM, Schmidt ML, Demuth DR. 2008. Induction of Aggregatibacter actinomycetemcomitans leukotoxin expression by IS1301 and orfA. Microbiology (Reading, Engl.). 154:528–538.
  • Schmid AK, Lipton MS, Mottaz H, Monroe ME, Smith RD, Lidstrom ME. 2005. Global whole-cell FTICR mass spectrometric proteomics analysis of the heat shock response in the radioresistant bacterium Deinococcus radiodurans. J Proteome Res. 4:709–718.
  • Schneider D, Duperchy E, Coursange E, Lenski RE, Blot M. 2000. Long-term experimental evolution in Escherichia coli. IX. Characterization of insertion sequence-mediated mutations and rearrangements. Genetics. 156:477–488.
  • Schneider D, Lenski RE. 2004. Dynamics of insertion sequence elements during experimental evolution of bacteria. Res Microbiol. 155:319–327.
  • Schnetz K, Rak B. 1992. IS5: a mobile enhancer of transcription in Escherichia coli. Proc Natl Acad Sci USA. 89:1244–1248.
  • Segal H, Nelson EC, Elisha BG. 2004. Genetic environment and transcription of ampC in an Acinetobacter baumannii clinical isolate. Antimicrob Agents Chemother. 48:612–614.
  • Shen MM, Raleigh EA, Kleckner N. 1987. Physical analysis of Tn10- and IS10-promoted transpositions and rearrangements. Genetics. 116:359–369.
  • Siguier P, Filee J, Chandler M. 2006. Insertion sequences in prokaryotic genomes. Curr Opin Microbiol. 9:526–531.
  • Siguier P, Gagnevin L, Chandler M. 2009. The new IS1595 family, its relation to IS1 and the frontier between insertion sequences and transposons. Res Microbiol. 160:232–241.
  • Siguier P, Gourbeyre E, Chandler M. 2014. Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev. FEMS Microbiol Rev. 38:865–891.
  • Siguier P, Gourbeyre E, Varani A, Ton-Hoang B, Chandler M. 2015. Everyman’s guide to bacterial insertion sequences. In: Mobile DNA III. Washington (DC): American Society of Microbiology.
  • Simons RW, Hoopes BC, McClure WR, Kleckner N. 1983. Three promoters near the termini of IS10: pIN, pOUT, and pIII. Cell 34:673–682.
  • Simpson AE, Skurray RA, Firth N. 2000. An IS257-derived hybrid promoter directs transcription of a tetA(K) tetracycline resistance gene in the Staphylococcus aureus chromosomal mec region. J Bacteriol. 182:3345–3352.
  • Simser JA, Rahman MS, Dreher-Lesnick SM, Azad AF. 2005. A novel and naturally occurring transposon, ISRpe1 in the Rickettsia peacockii genome disrupting the rickA gene involved in actin-based motility. Mol Microbiol. 58:71–79.
  • Skaugen M, Nes IF. 1994. Transposition in Lactobacillus sake and its abolition of lactocin S production by insertion of IS1163, a new member of the IS3 family. Appl Environ Microbiol. 60:2818–2825.
  • Skaugen M, Nes IF. 2000. Transposition in Lactobacillus sakei: inactivation of a second lactocin S operon by the insertion of IS1520, a new member of the IS3 family of insertion sequences. Microbiology. 146:1163–1169.
  • Snesrud E, He S, Chandler M, Dekker JP, Hickman AB, McGann P, Dyda F. 2016. A model for transposition of the colistin resistance gene mcr-1 by ISApl1. Antimicrob Agents Chemother. 60:6973–6976.
  • Sobrero P, Valverde C. 2012. The bacterial protein Hfq: much more than a mere RNA-binding factor. Crit Rev Microbiol. 38:276–299.
  • Soki J, Gal M, Brazier JS, Rotimi VO, Urban E, Nagy E, Duerden BI. 2006. Molecular investigation of genetic elements contributing to metronidazole resistance in Bacteroides strains. J Antimicrob Chemother. 57:212–220.
  • Sousa A, Bourgard C, Wahl LM, Gordo I. 2013. Rates of transposition in Escherichia coli. Biol Lett. 9:20130838.
  • Stinear TP, Seemann T, Pidot S, Frigui W, Reysset G, Garnier T, Meurice G, Simon D, Bouchier C, Ma L, et al. 2007. Reductive evolution and niche adaptation inferred from the genome of Mycobacterium ulcerans, the causative agent of Buruli ulcer. Genome Res. 17:192–200.
  • Sun X, Dennis JJ. 2009. A novel insertion sequence derepresses efflux pump expression and preadapts Pseudomonas putida S12 for extreme solvent stress. J Bacteriol. 191:6773–6777.
  • Szeverenyi I, Nagy Z, Farkas T, Olasz F, Kiss J. 2003. Detection and analysis of transpositionally active head-to-tail dimers in three additional Escherichia coli IS elements. Microbiology (Reading, Engl.). 149:1297–1310.
  • Takahashi K, Sekine Y, Chibazakura T, Yoshikawa H. 2007. Development of an intermolecular transposition assay system in Bacillus subtilis 168 using IS4Bsu1 from Bacillus subtilis (natto). Microbiology (Reading, Engl.). 153:2553–2559.
  • Tanaka KH, Dallaire-Dufresne S, Daher RK, Frenette M, Charette SJ. 2012. An insertion sequence-dependent plasmid rearrangement in Aeromonas salmonicida causes the loss of the type three secretion system. PLoS One. 7:e33725.
  • Tibazarwa C, Wuertz S, Mergeay M, Wyns L, van der Lelie D. 2000. Regulation of the cnr cobalt and nickel resistance determinant of Ralstonia eutropha (Alcaligenes eutrophus) CH34. J Bacteriol. 182:1399–1409.
  • Tolmasky ME, Crosa JH. 1995. Iron transport genes of the pJM1-mediated iron uptake system of Vibrio anguillarum are included in a transposonlike structure. Plasmid. 33:180–190.
  • Treves DS, Manning S, Adams J. 1998. Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol. 15:789–797.
  • Trinh S, Haggoud A, Reysset G, Sebald M. 1995. Plasmids Pip419 and Pip421 from Bacteroides – 5-nitroimidazole resistance genes and their upstream insertion-sequence elements. Microbiology-UK. 141:927–935.
  • Turton JF, Ward ME, Woodford N, Kaufmann ME, Pike R, Livermore DM, Pitt TL. 2006. The role of ISAba1 in expression of OXA carbapenemase genes in Acinetobacter baumannii. FEMS Microbiol Lett. 258:72–77.
  • Twiss E, Coros AM, Tavakoli NP, Derbyshire KM. 2005. Transposition is modulated by a diverse set of host factors in Escherichia coli and is stimulated by nutritional stress. Mol Microbiol. 57:1593–1607.
  • Twomey DP, McKAy LL, O'Sullivan DJ. 1998. Molecular characterization of the Lactococcus lactis LlaKR2I restriction-modification system and effect of an IS982 element positioned between the restriction and modification genes. J Bacteriol. 180:5844–5854.
  • van der Ploeg J, Willemsen M, van Hall G, Janssen DB. 1995. Adaptation of Xanthobacter autotrophicus GJ10 to bromoacetate due to activation and mobilization of the haloacetate dehalogenase gene by insertion element IS1247. J Bacteriol. 177:1348–1356.
  • Vandecraen J, Monsieurs P, Mergeay M, Leys N, Aertsen A, Van Houdt R. 2016. Zinc-induced transposition of insertion sequence elements contributes to increased adaptability of Cupriavidus metallidurans. Front Microbiol. 7:359.
  • Vogel J, Bartels V, Tang TH, Churakov G, Slagter-Jager JG, Huttenhofer A, Wagner EG. 2003. RNomics in Escherichia coli detects new sRNA species and indicates parallel transcriptional output in bacteria. Nucleic Acids Res. 31:6435–6443.
  • Vogel J, Luisi BF. 2011. Hfq and its constellation of RNA. Nat Rev Microbiol. 9:578–589.
  • Wachino J, Yamane K, Kimura K, Shibata N, Suzuki S, Ike Y, Arakawa Y. 2006. Mode of transposition and expression of 16S rRNA methyltransferase gene rmtC accompanied by ISEcp1. Antimicrob Agents Chemother. 50:3212–3215.
  • Wang A, Roth JR. 1988. Activation of silent genes by transposons Tn5 and Tn10. Genetics 120:875–885.
  • Wery J, Hidayat B, Kieboom J, de Bont JA. 2001. An insertion sequence prepares Pseudomonas putida S12 for severe solvent stress. J Biol Chem. 276:5700–5706.
  • Wolter DJ, Hanson ND, Lister PD. 2004. Insertional inactivation of oprD in clinical isolates of Pseudomonas aeruginosa leading to carbapenem resistance. FEMS Microbiol Lett. 236:137–143.
  • Wood MS, Byrne A, Lessie TG. 1991. IS406 and IS407, two gene-activating insertion sequences for Pseudomonas cepacia. Gene. 105:101–105.
  • Wu Y, Aandahl RZ, Tanaka MM. 2015. Dynamics of bacterial insertion sequences: can transposition bursts help the elements persist? BMC Evol Biol. 15:288.
  • Zambrano MM, Siegele DA, Almiron M, Tormo A, Kolter R. 1993. Microbial competition: Escherichia coli mutants that take over stationary phase cultures. Science 259:1757–1760.
  • Zerbib D, Polard P, Escoubas JM, Galas D, Chandler M. 1990. The regulatory role of the IS1-encoded InsA protein in transposition. Mol Microbiol. 4:471–477.
  • Zhang Z, Saier MH. Jr. 2009a. A mechanism of transposon-mediated directed mutation. Mol Microbiol. 74:29–43.
  • Zhang Z, Saier MH. Jr. 2009b. A novel mechanism of transposon-mediated gene activation. PLoS Genet. 5:e1000689.
  • Ziebuhr W, Krimmer V, Rachid S, Lossner I, Gotz F, Hacker J. 1999. A novel mechanism of phase variation of virulence in Staphylococcus epidermidis: evidence for control of the polysaccharide intercellular adhesin synthesis by alternating insertion and excision of the insertion sequence element IS256. Mol Microbiol. 32:345–356.
  • Zinser ER, Schneider D, Blot M, Kolter R. 2003. Bacterial evolution through the selective loss of beneficial genes. Trade-offs in expression involving two loci. Genetics. 164:1271–1277.