1887

Chapter 6 : The Integron: Adaptation On Demand

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

The Integron: Adaptation On Demand, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555819217/9781555819200_Chap06-1.gif /docserver/preview/fulltext/10.1128/9781555819217/9781555819200_Chap06-2.gif

Abstract:

Integrons are genetic platforms that allow bacteria to evolve rapidly through the acquisition, stockpiling, excision, and reordering of open reading frames found in mobile elements named cassettes. The evolutionary potency that integrons provide for bacteria is based on the variety of functions encoded in the cassettes, as well as on the intricate coupling of integron activity to bacterial stress ( ).

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0019-2014

Key Concept Ranking

DNA Synthesis
0.6454825
Genetic Elements
0.56479716
DNA Damage and Repair
0.43717152
Horizontal Gene Transfer
0.41551813
0.6454825
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Image of Figure 1
Figure 1

Organization of integrons. (A) Insertion and excision of cassettes: the functional platform, composed of the integrase-encoding gene, the cassette (P) and integrase promoters (Pint), and the primary recombination site (red triangle), is shown. Cassette insertion ( × ) and excision ( ×  catalyzed by the IntI integrase are represented. Hybrid and sites are indicated. Arrows inside the cassettes indicate the direction of the open reading frame. (B) Expression of cassettes: cassettes of the array are represented by small arrows. Their expression level is reflected by the color intensity of each arrow. Only the first cassettes of the array are expressed, and the subsequent ones can be seen as a low-cost cassette reservoir. doi:10.1128/microbiolspec.MDNA3-0019-2014.f1

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0019-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 2
Figure 2

Integron recombination sites. The putative IntI1 binding domains are marked with green boxes. The black arrows show the cleavage points. (A) Sequence of the double-stranded site: inverted repeats (R and L) and direct repeats (DR1 and DR2) are indicated with gray arrows. (B) Schematic representation of double-stranded (ds) sites; inverted repeats (R”, L” L’, and R’) are indicated with gray arrows. The dotted lines represent the variable central part. The conserved nucleotides are indicated. Asterisks (*) show the conserved G nucleotides, which generate extrahelical bases (EHB) in the folded site bottom strand (bs). The top strand (ts) and bottom strand (bs) are marked. (C) Proposed secondary structures of the and VCR bottom strands: structures were determined by the UNAFOLD online interface at the Institut Pasteur. Structural features of sites, namely, the Unpaired Central Spacer (UCS), the ExtraHelical Bases (EHBs), the stem and the Variable Terminal Structure (VTS) are indicated. Asterisks (*) show the conserved G extrahelical base. The conserved triplet (CT) is indicated. Primary sequences of the sites are shown (except for the VTS of the VCR site). (D) Schematic representation of structural features of the VCR site and their roles: the structural features and their roles are indicated. doi:10.1128/microbiolspec.MDNA3-0019-2014.f2

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0019-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 3
Figure 3

Replicative resolution of integron cassette insertion. Recombination between a double-stranded site (bold red lines) and a single-stranded bottom site (bold green lines) terminating a cassette is shown. The top strand of the site is represented as a dotted line because we do not exactly know the nature of the cassettes (ss or ds). The synaptic complex comprises two DNA duplexes bound by four integrase protomers. The two activated protomers are represented by dark gray ovals. One strand from each duplex is cleaved and transferred to form an atypical Holliday junction (aHJ). Classical resolution gives rise to covalently closed abortive molecules. The non-abortive resolution implies a replication step. The origin of replication is represented by a purple circle and the newly synthesized leading and lagging strands by dashed purple lines. Both products are represented: the initial substrate resulting from the top strand replication, and the molecule containing the inserted cassette resulting from the bottom strand replication. Hybrid and sites are indicated. doi:10.1128/microbiolspec.MDNA3-0019-2014.f3

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0019-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 4
Figure 4

Replicative resolution model of integron cassette excision. Recombination between two single-stranded bottom sites (bold green and pink lines) is shown. Top strands of sites are represented as dotted lines. The synaptic complex comprises two DNA duplexes bound by four integrase protomers. The two activated protomers are represented by dark gray ovals. One strand from each duplex is cleaved and transferred to form an atypical Holliday junction (aHJ). The proposed aHJ resolution model implying a replication step is based on the  ×  recombination. The origin of replication is represented by a purple circle and the newly synthesized leading and lagging strands by dashed purple lines. Products are represented: on one hand, the initial substrate resulting from the top strand replication, and on the other, the excised cassette (cassette) and the molecule devoid of the excised cassette (cassette 2 excised) both resulting from the bottom strand replication. Hybrid sites are indicated. doi:10.1128/microbiolspec.MDNA3-0019-2014.f4

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0019-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 5
Figure 5

Two resolution pathways proposed for  ×  recombination. Recombination between two double-stranded sites (bold green and pink lines) is shown. The first proposed pathway is similar to the classical site-specific recombination catalyzed by Y-recombinases. The synaptic complex comprises two DNA duplexes bound by four recombinase protomers. The first two activated protomers are represented by dark gray ovals. One strand from each duplex is cleaved and transferred to form a HJ. Isomerization of this junction alternates the catalytic activity between the two pairs of protomers (dark and light-gray ovals) ensuring the second strand exchange and recombination product formation (co-integrate). The second pathway proposes a resolution of the HJ by replication. The origin of replication is represented by a purple circle and the newly synthesized leading and lagging strands by dashed purple lines. Products are represented: two initial substrates resulting from the top strand replication and co-integrate resulting from the bottom strand replication. Hybrid sites are indicated. doi:10.1128/microbiolspec.MDNA3-0019-2014.f5

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0019-2014
Permissions and Reprints Request Permissions
Download as Powerpoint
Image of Figure 6
Figure 6

Intimate connection between the integron and cell physiology. A snapshot representation of the links between integrons’ activity and bacterial physiology is shown. The main triggering signal for integrase expression is the bacterial SOS response. A detailed description of these connections is depicted in the section entitled: doi:10.1128/microbiolspec.MDNA3-0019-2014.f6

Citation: Escudero* J, Loot* C, Nivina A, Mazel D. 2015. The Integron: Adaptation On Demand, p 139-161. In Craig N, Chandler M, Gellert M, Lambowitz A, Rice P, Sandmeyer S (ed), Mobile DNA III. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MDNA3-0019-2014
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781555819217.chap6
1. Stokes HW,, Hall RM . 1989. A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol Microbiol 3 : 16691683.[PubMed] [CrossRef]
2. Jové T,, Da Re S,, Denis F,, Mazel D,, Ploy MC . 2010. Inverse correlation between promoter strength and excision activity in class 1 integrons. PLoS Genet 6 : e1000793. [PubMed] [CrossRef]
3. Levesque C,, Brassard S,, Lapointe J,, Roy PH . 1994. Diversity and relative strength of tandem promoters for the antibiotic-resistance genes of several integrons. Gene 142 : 4954.[PubMed] [CrossRef]
4. Collis CM,, Hall RM . 1995. Expression of antibiotic resistance genes in the integrated cassettes of integrons. Antimicrob Agents Chemother 39 : 155162.[PubMed] [CrossRef]
5. Collis CM,, Hall RM . 1992. Gene cassettes from the insert region of integrons are excised as covalently closed circles. Mol Microbiol 6 : 28752885.[PubMed] [CrossRef]
6. Rowe-Magnus DA,, Guerout AM,, Ploncard P,, Dychinco B,, Davies J,, Mazel D . 2001. The evolutionary history of chromosomal super-integrons provides an ancestry for multiresistant integrons. Proc Natl Acad Sci U S A 98 : 652657.[PubMed] [CrossRef]
7. Cambray G,, Guerout AM,, Mazel D . 2010. Integrons. Annu Rev Genet 44 : 141166.[PubMed] [CrossRef]
8. Nemergut DR,, Robeson MS,, Kysela RF,, Martin AP,, Schmidt SK,, Knight R . 2008. Insights and inferences about integron evolution from genomic data. BMC genomics 9 : 261. [PubMed] [CrossRef]
9. Cambray G,, Mazel D . 2008. Synonymous genes explore different evolutionary landscapes. PLoS Genet 4(11): e1000256. [PubMed] [CrossRef]
10. Boucher Y,, Labbate M,, Koenig JE,, Stokes HW . 2007. Integrons: mobilizable platforms that promote genetic diversity in bacteria. Trends Microbiol 15 : 301309.[PubMed] [CrossRef]
11. Mazel D . 2006. Integrons: agents of bacterial evolution. Nature RevMicrobiol 4 : 608620.[PubMed] [CrossRef]
12. Mazel D,, Dychinco B,, Webb VA,, Davies J . 1998. A distinctive class of integron in the Vibrio cholerae genome. Science 280 : 605608.[PubMed] [CrossRef]
13. Ogawa A,, Takeda T . 1993. The gene encoding the heat-stable enterotoxin of Vibrio cholerae is flanked by 123-base pair direct repeats. Microbiol Immunol 37 : 607616.[PubMed] [CrossRef]
14. Barker A,, Clark CA,, Manning PA . 1994. Identification of VCR, a repeated sequence associated with a locus encoding a hemagglutinin in Vibrio cholerae O1. J Bacteriol 176 : 54505458.[PubMed]
15. Rowe-Magnus DA,, Guerout AM,, Biskri L,, Bouige P,, Mazel D . 2003. Comparative analysis of superintegrons: engineering extensive genetic diversity in the Vibrionaceae. Genome Res 13 : 428442.[PubMed] [CrossRef]
16. Mitsuhashi S,, Harada K,, Hashimoto H,, Egawa R . 1961. On the drug-resistance of enteric bacteria. 4. Drug-resistance of Shigella prevalent in Japan. Jpn J Exp Med 31 : 4752.[PubMed]
17. Martinez E,, de la Cruz F . 1988. Transposon Tn21 encodes a RecA-independent site-specific integration system. Mol Gen Genet 211 : 320325.[PubMed] [CrossRef]
18. Arakawa Y,, Murakami M,, Suzuki K,, Ito H,, Wacharotayankun R,, Ohsuka S,, Kato N,, Ohta M . 1995. A novel integron-like element carrying the metallo-beta-lactamase gene blaIMP. Antimicrob Agents Chemother 39 : 16121615.[PubMed] [CrossRef]
19. Collis CM,, Kim MJ,, Partridge SR,, Stokes HW,, Hall RM . 2002. Characterization of the Class 3 integron and the site-specific recombination system it determines. J Bacteriol 184 : 30173026.[PubMed] [CrossRef]
20. Xu H,, Davies J,, Miao V . 2007. Molecular characterization of class 3 integrons from Delftia spp. J Bacteriol 189 : 6276683.[PubMed] [CrossRef]
21. Ramírez MS,, Piñeiro S,, Centrón D . 2010. Novel insights about class 2 integrons from experimental and genomic epidemiology. Antimicrob Agents Chemother 54 : 699706.[PubMed] [CrossRef]
22. Hochhut B,, Lotfi Y,, Mazel D,, Faruque SM,, Woodgate R,, Waldor MK . 2001. Molecular analysis of antibiotic resistance gene clusters in Vibrio cholerae O139 and O1 SXT constins. Antimicrob Agents Chemother 45 : 29913000.[PubMed] [CrossRef]
23. Sørum H,, Roberts MC,, Crosa JH . 1992. Identification and cloning of a tetracycline resistance gene from the fish pathogen Vibrio salmonicida . Antimicrob Agents Chemother. 36 : 611615.[PubMed] [CrossRef]
24. Naas T,, Mikami Y,, Imai T,, Poirel L,, Nordmann P . 2001. Characterization of In53, a class 1 plasmid- and composite transposon-located integron of Escherichia coli which carries an unusual array of gene cassettes. J Bacteriol 183 : 235249.[PubMed] [CrossRef]
25. Partridge SR,, Tsafnat G,, Coiera E,, Iredell JR . 2009. Gene cassettes and cassette arrays in mobile resistance integrons. FEMS Microbiol Rev 33 : 757784.[PubMed] [CrossRef]
26. Fluit AC,, Schmitz FJ . 2004. Resistance integrons and super-integrons. Clin Microbiol Infect 10 : 272288.[PubMed] [CrossRef]
27. Labbate M,, Case RJ,, Stokes HW . 2009. The integron/gene cassette system: an active player in bacterial adaptation. Methods Mol Biol 532 : 103125.[PubMed] [CrossRef]
28. Martin C,, Timm J,, Rauzier J,, Gomez-Lus R,, Davies J,, Gicquel B . 1990. Transposition of an antibiotic resistance element in mycobacteria. Nature 345 : 739743.[PubMed] [CrossRef]
29. Nandi S,, Maurer JI,, Hofacre C,, Summers AO . 2004. Gram-positive bacteria are a major reservoir of Class 1 antibiotic resistance integrons in poultry litter. Proc Natl Acad Sci USA 101 : 71187122.[PubMed] [CrossRef]
30. Nesvera J,, Hochmannová J,, Pátek M . 1998. An integron of class 1 is present on the plasmid pCG4 from gram-positive bacterium Corynebacterium glutamicum . FEMS Microbiol Lett 169 : 391395.[PubMed] [CrossRef]
31. Shi L,, Zheng M,, Xiao Z,, Asakura M,, Su J,, Li L,, Yamasaki S . 2006. Unnoticed spread of class 1 integrons in gram-positive clinical strains isolated in Guangzhou, China. Microbiol Immunol 50 : 463467.[PubMed] [CrossRef]
32. Hocquet D,, Llanes C,, Thouverez M,, Kulasekara HD,, Bertrand X,, Plésiat P,, Mazel D,, Miller SI . 2012. Evidence for induction of integron-based antibiotic resistance by the SOS response in a clinical setting. PLoS Pathog 8 : e1002778. [PubMed] [CrossRef]
33. Gravel A,, Fournier B,, Roy PH . 1998. DNA complexes obtained with the integron integrase IntI1 at the attI1 site. Nucleic Acids Res 26 : 43474355.[PubMed] [CrossRef]
34. Partridge SR,, Recchia GD,, Scaramuzzi C,, Collis CM,, Stokes HW,, Hall RM . 2000. Definition of the attI1 site of class 1 integrons. Microbiology 146 : 28552864.[PubMed]
35. Nield BS,, Holmes AJ,, Gillings MR,, Recchia GD,, Mabbutt BC,, Nevalainen KM,, Stokes HW . 2001. Recovery of new integron classes from environmental DNA. FEMS Microbiol Lett 195 : 5965.[PubMed] [CrossRef]
36. Elsaied H,, Stokes HW,, Kitamura K,, Kurusu Y,, Kamagata Y,, Maruyama A . 2011. Marine integrons containing novel integrase genes, attachment sites, attI, and associated gene cassettes in polluted sediments from Suez and Tokyo Bays. ISME J 5 : 11621177.[PubMed] [CrossRef]
37. Biskri L,, Bouvier M,, Guérout AM,, Boisnard S,, Mazel D . 2005. Comparative study of class 1 integron and Vibrio cholerae superintegron integrase activities. J Bacteriol 187 : 17401750.[PubMed] [CrossRef]
38. Stokes HW,, O’Gorman DB,, Recchia GD,, Parsekhian M,, Hall RM . 1997. Structure and function of 59-base element recombination sites associated with mobile gene cassettes. Mol Microbiol 26 : 731745.[PubMed] [CrossRef]
39. Hall RM,, Brookes DE,, Stokes HW . 1991. Site-specific insertion of genes into integrons: role of the 59-base element and determination of the recombination cross-over point. Mol Microbiol 5 : 19411959.[PubMed] [CrossRef]
40. Francia MV,, Zabala JC,, de la Cruz F,, García Lobo JM . 1999. The IntI1 integron integrase preferentially binds single-stranded DNA of the attC site. J Bacteriol 181 : 68446849.[PubMed]
41. Johansson C,, Kamali-Moghaddam M,, Sundstrom L . 2004. Integron integrase binds to bulged hairpin DNA. Nucleic Acids Res 32 : 40334043.[PubMed] [CrossRef]
42. Bouvier M,, Demarre G,, Mazel D . 2005. Integron cassette insertion: a recombination process involving a folded single strand substrate. EMBO J 24 : 43564367.[PubMed] [CrossRef]
43. Bouvier M,, Ducos-Galand M,, Loot C,, Bikard D,, Mazel D . 2009. Structural features of single-stranded integron cassette attC sites and their role in strand selection. PLoS Genetics 5 : e1000632. [PubMed] [CrossRef]
44. MacDonald D,, Demarre G,, Bouvier M,, Mazel D,, Gopaul DN . 2006. Structural basis for broad DNA-specificity in integron recombination. Nature 440 : 11571162.[PubMed] [CrossRef]
45. Loot C,, Bikard D,, Rachlin A,, Mazel D . 2010. Cellular pathways controlling integron cassette site folding. EMBO J 29 : 26232634.[PubMed] [CrossRef]
46. Nunes-Düby SE,, Kwon HJ,, Tirumalai RS,, Ellenberger T,, Landy A . 1998. Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res 26 : 391406.[PubMed] [CrossRef]
47. Boyd EF,, Almagro-Moreno S,, Parent MA . 2009. Genomic islands are dynamic, ancient integrative elements in bacterial evolution. Trends Microbiol 17 : 4753.[PubMed] [CrossRef]
48. Grindley N,, Whiteson K,, Rice P . 2006. Mechanisms of site-specific recombination. Annu Rev Biochem 75 : 567605.[PubMed] [CrossRef]
49. Messier N,, Roy PH . 2001. Integron integrases possess a unique additional domain necessary for activity. J Bacteriol 183 : 66996706.[PubMed] [CrossRef]
50. Demarre G,, Frumerie C,, Gopaul DN,, Mazel D . 2007. Identification of key structural determinants of the IntI1 integron integrase that influence attC × attI1 recombination efficiency. Nucleic Acids Res 35 : 64756489.[PubMed] [CrossRef]
51. Gravel A,, Messier N,, Roy PH . 1998. Point mutations in the integron integrase IntI1 that affect recombination and/or substrate recognition. J Bacteriol 180 : 54375442.[PubMed]
52. Johansson C,, Boukharta L,, Eriksson J,, Aqvist J,, Sundström L . 2009. Mutagenesis and homology modeling of the Tn21 integron integrase IntI1. Biochemistry 48 : 17431753.[PubMed] [CrossRef]
53. Val ME,, Bouvier M,, Campos J,, Sherratt D,, Cornet F,, Mazel D,, Barre FX . 2005. The single-stranded genome of phage CTX is the form used for integration into the genome of Vibrio cholerae . Mol Cell 19 : 559566.[PubMed] [CrossRef]
54. Loot C,, Ducos-Galand M,, Escudero JA,, Bouvier M,, Mazel D . 2012. Replicative resolution of integron cassette insertion. Nucleic Acids Res 40 : 83618370.[PubMed] [CrossRef]
55. Loot C,, Parissi V,, Escudero JA,, Amarir-Bouhram J,, Bikard D,, Mazel D . 2014. The integron integrase efficiently prevents the melting effect of Escherichia coli single-stranded DNA-binding protein on folded attC sites. J Bacteriol 196 : 762771.[PubMed] [CrossRef]
56. Collis CM,, Grammaticopoulos G,, Briton J,, Stokes HW,, Hall RM . 1993. Site-specific insertion of gene cassettes into integrons. Mol Microbiol 9 : 4152.[PubMed] [CrossRef]
57. Collis CM,, Recchia GD,, Kim MJ,, Stokes HW,, Hall RM . 2001. Efficiency of recombination reactions catalyzed by class 1 integron integrase IntI1. J Bacteriol 183 : 25352542.[PubMed] [CrossRef]
58. Baharoglu Z,, Bikard D,, Mazel D . 2010. Conjugative DNA transfer induces the bacterial SOS response and promotes antibiotic resistance development through integron activation. PLoS Genet 6 : e1001165. [PubMed] [CrossRef]
59. Collis CM,, Hall RM . 1992. Site-specific deletion and rearrangement of integron insert genes catalyzed by the integron DNA integrase. J Bacteriol 174 : 15741585.[PubMed]
60. Gestal AM,, Stokes HW,, Partridge SR,, Hall RM . 2005. Recombination between the dfrA12-orfF-aadA2 cassette array and an aadA1 gene cassette creates a hybrid cassette, aadA8b. Antimicrob Agents Chemother 49 : 47714774.[PubMed] [CrossRef]
61. Hansson K,, Sköld O,, Sundström L . 1997. Non-palindromic attl sites of integrons are capable of site-specific recombination with one another and with secondary targets. Mol Microbiol 26 : 441453.[PubMed] [CrossRef]
62. Roy Chowdhury P,, Merlino J,, Labbate M,, Cheong EY,, Gottlieb T,, Stokes HW . 2009. Tn6060, a transposon from a genomic island in a Pseudomonas aeruginosa clinical isolate that includes two class 1 integrons. Antimicrob Agents Chemother 53 : 52945296.[PubMed] [CrossRef]
63. González-Zorn B,, Catalan A,, Escudero JA,, Domínguez L,, Teshager T,, Porrero C,, Moreno MA . 2005. Genetic basis for dissemination of armA. J Antimicrob Chemother 56 : 583585.[PubMed] [CrossRef]
64. Recchia GD,, Hall RM . 1995. Plasmid evolution by acquisition of mobile gene cassettes: plasmid pIE723 contains the aadB gene cassette precisely inserted at a secondary site in the incQ plasmid RSF1010. Mol Microbiol 15 : 179187.[PubMed] [CrossRef]
65. Segal H,, Francia MV,, Lobo JM,, Elisha G . 1999. Reconstruction of an active integron recombination site after integration of a gene cassette at a secondary site. Antimicrob Agents Chemother 43 : 25382541.[PubMed]
66. Jacquier H,, Zaoui C,, Sanson-le Pors MJ,, Mazel D,, Berçot B . 2009. Translation regulation of integrons gene cassette expression by the attC sites. Mol Microbiol 72 : 14751486.[PubMed] [CrossRef]
67. Shultzaberger RK,, Bucheimer RE,, Rudd KE,, Schneider TD . 2001. Anatomy of Escherichia coli ribosome binding sites. J Mol Biol 313 : 215228.[PubMed] [CrossRef]
68. Hanau-Berçot B,, Podglajen I,, Casin I,, Collatz E . 2002. An intrinsic control element for translational initiation in class 1 integrons. Mol Microbiol 44 : 119130.[PubMed] [CrossRef]
69. Bissonnette L,, Champetier S,, Buisson JP,, Roy PH . 1991. Characterization of the nonenzymatic chloramphenicol resistance (cmlA) gene of the In4 integron of Tn1696: similarity of the product to transmembrane transport proteins. J Bacteriol 173 : 44934502.[PubMed]
70. Stokes HW,, Hall RM . 1991. Sequence analysis of the inducible chloramphenicol resistance determinant in the Tn1696 integron suggests regulation by translational attenuation. Plasmid 26 : 1019.[PubMed] [CrossRef]
71. Biskri L,, Mazel D . 2003. Erythromycin esterase gene ere(A) is located in a functional gene cassette in an unusual class 2 integron. Antimicrob Agents Chemother 47 : 33263331.[PubMed] [CrossRef]
72. da Fonseca ÉL,, Vicente AC . 2012. Functional characterization of a Cassette-specific promoter in the class 1 integron-associated qnrVC1 gene. Antimicrob Agents Chemother 56 : 33923394.[PubMed] [CrossRef]
73. Szekeres S,, Dauti M,, Wilde C,, Mazel D,, Rowe-Magnus DA . 2007. Chromosomal toxin-antitoxin loci can diminish large-scale genome reductions in the absence of selection. Mol Microbiol 63 : 15881605.[PubMed] [CrossRef]
74. Guérout AM,, Iqbal N,, Mine N,, Ducos-Galand M,, Van Melderen L,, Mazel D . 2013. Characterization of the phd-doc and ccd toxin-antitoxin cassettes from Vibrio superintegrons. J Bacteriol 195 : 22702283.[PubMed] [CrossRef]
75. Elsaied H,, Stokes HW,, Nakamura T,, Kitamura K,, Fuse H,, Maruyama A . 2007. Novel and diverse integron integrase genes and integron-like gene cassettes are prevalent in deep-sea hydrothermal vents. Environ Microbiol 9 : 22982312.[PubMed] [CrossRef]
76. Stokes HW,, Holmes AJ,, Nield BS,, Holley MP,, Nevalainen KM,, Mabbutt BC,, Gillings MR . 2001. Gene cassette PCR: sequence-independent recovery of entire genes from environmental DNA. Appl Environ Microbiol 67 : 52405246.[PubMed] [CrossRef]
77. Koenig JE,, Boucher Y,, Charlebois RL,, Nesbø C,, Zhaxybayeva O,, Bapteste E,, Spencer M,, Joss MJ,, Stokes HW,, Doolittle WF . 2008. Integron-associated gene cassettes in Halifax Harbour: assessment of a mobile gene pool in marine sediments. Environ Microbiol 10 : 10241038.[PubMed] [CrossRef]
78. Gillings MR,, Holley MP,, Stokes HW . 2009. Evidence for dynamic exchange of qac gene cassettes between class 1 integrons and other integrons in freshwater biofilms. FEMS Microbiol Lett 296 : 282288.[PubMed] [CrossRef]
79. Holmes AJ,, Gillings MR,, Nield BS,, Mabbutt BC,, Nevalainen KM,, Stokes HW . 2003. The gene cassette metagenome is a basic resource for bacterial genome evolution. Environ Microbiol 5 : 383394.[PubMed] [CrossRef]
80. Gillings M,, Boucher Y,, Labbate M,, Holmes A,, Krishnan S,, Holley M,, Stokes HW . 2008. The evolution of class 1 integrons and the rise of antibiotic resistance. J Bacteriol 190 : 50955100.[PubMed] [CrossRef]
81. Gillings MR,, Holley MP,, Stokes HW,, Holmes AJ . 2005. Integrons in Xanthomonas: a source of speciesgenome diversity. Proc Natl Acad Sci USA 102 : 44194424.[PubMed] [CrossRef]
82. Rapa RA,, Labbate M . 2013. The function of integron-associated gene cassettes in Vibrio species: the tip of the iceberg. Front Microbiol 4 : 385. [PubMed] [CrossRef]
83. Gerdes K,, Christensen SK,, Lobner-Olesen A . 2005. Prokaryotic toxin-antitoxin stress response loci. Nat Rev Microbiol 3 : 371382.[PubMed] [CrossRef]
84. Yamaguchi Y,, Park JH,, Inouye M . 2011. Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 45 : 6179.[PubMed] [CrossRef]
85. Van Melderen L,, Saavedra De Bast M . 2009. Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genetics 5 : e1000437. [PubMed] [CrossRef]
86. Sberro H,, Leavitt A,, Kiro R,, Koh E,, Peleg Y,, Qimron U,, Sorek R . 2013. Discovery of functional toxin/antitoxin systems in bacteria by shotgun cloning. Molecular Cell 50 : 136148.[PubMed] [CrossRef]
87. Tsafnat G,, Copty J,, Partridge SR . 2011. RAC: Repository of Antibiotic resistance Cassettes. Database: the journal of biological databases and curation. 2011:bar054. [PubMed] [CrossRef]
88. Moura A,, Soares M,, Pereira C,, Leitão N,, Henriques I,, Correia A . 2009. INTEGRALL: a database and search engine for integrons, integrases and gene cassettes. Bioinformatics 25 : 10961098.[PubMed] [CrossRef]
89. Joss MJ,, Koenig JE,, Labbate M,, Polz MF,, Gillings MR,, Stokes HW,, Doolittle WF,, Boucher Y . 2009. ACID: annotation of cassette and integron data. BMC Bioinformatics 10 : 118. [PubMed] [CrossRef]
90. Rowe-Magnus DA,, Guérout AM,, Mazel D . 1999. Super-integrons. Res Microbiol 150 : 641651.[PubMed] [CrossRef]
91. Chowdhury N,, Asakura M,, Neogi SB,, Hinenoya A,, Haldar S,, Ramamurthy T,, Sarkar BL,, Faruque SM,, Yamasaki S . 2010. Development of simple and rapid PCR-fingerprinting methods for Vibrio cholerae on the basis of genetic diversity of the superintegron. J Appl Microbiol 109 : 304312.[PubMed]
92. Feng L,, Reeves PR,, Lan R,, Ren Y,, Gao C,, Zhou Z,, Cheng J,, Wang W,, Wang J,, Qian W,, Li D,, Wang L . 2008. A recalibrated molecular clock and independent origins for the cholera pandemic clones. PloS One 3 : e4053. [PubMed] [CrossRef]
93. Labbate M,, Boucher Y,, Joss MJ,, Michael CA,, Gillings MR,, Stokes HW . 2007. Use of chromosomal integron arrays as a phylogenetic typing system for Vibrio cholerae pandemic strains. Microbiology 153 : 14881498.[PubMed] [CrossRef]
94. Erill I,, Campoy S,, Barbé J . 2007. Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol Rev 31 : 637656.[PubMed] [CrossRef]
95. Guerin E,, Cambray G,, Sanchez-Alberola N,, Campoy S,, Erill I,, Da Re S,, Gonzalez-Zorn B,, Barbe J,, Ploy MC,, Mazel D . 2009. The SOS response controls integron recombination. Science 324 : 1034. [PubMed] [CrossRef]
96. Cambray G,, Sanchez-Alberola N,, Campoy S,, Guerin E,, Da Re S,, González-Zorn B,, Ploy MC,, Barbe J,, Mazel D,, Erill I . 2011. Prevalence of SOS-mediated control of integron integrase expression as an adaptive trait of chromosomal and mobile integrons. Mob DNA 2 : 6. [PubMed] [CrossRef]
97. Harms K,, Starikova I,, Johnsen PJ . 2013. Costly Class-1 integrons and the domestication of the the functional integrase. Mobile Genetic Elements 3:e24774. [PubMed] [CrossRef]
98. Starikova I,, Harms K,, Haugen P,, Lunde T,, Primicerio R,, Samuelsen Ø,, Nielsen KM,, Johnsen PJ . 2012. A trade-off between the fitness cost of functional integrases and long-term stability of integrons. PLoS pathogens 8 : e1003043. [PubMed] [CrossRef]
99. Baharoglu Z,, Mazel D . 2011. Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance. Antimicrob Agents Chemother 55 : 24382441.[PubMed] [CrossRef]
100. Baharoglu Z,, Krin E,, Mazel D . 2013. RpoS plays a central role in the SOS induction by sub-lethal aminoglycoside concentrations in Vibrio cholerae . PLoS Genetics 9 : e1003421. [PubMed] [CrossRef]
101. Gutierrez A,, Laureti L,, Crussard S,, Abida H,, Rodríguez-Rojas A,, Blázquez J,, Baharoglu Z,, Mazel D,, Darfeuille F,, Vogel J,, Matic I . 2013. β-Lactam antibiotics promote bacterial mutagenesis via an RpoS-mediatedreduction in replication fidelity. Nature Commun 4 : 1610. [PubMed] [CrossRef]
102. Baharoglu Z,, Krin E,, Mazel D . 2012. Connecting environment and genome plasticity in the characterization of transformation-induced SOS regulation and carbon catabolite control of the Vibrio cholerae integron integrase. J Bacteriol 194 : 16591667.[PubMed] [CrossRef]
103. Krin E,, Cambray G,, Mazel D . 2014. The superintegron integrase and the cassette promoters are co-regulated in Vibrio cholerae . PLoS One 9 : e91194. [PubMed] [CrossRef]
104. Guérin E,, Jové T,, Tabesse A,, Mazel D,, Ploy MC . 2011. High-level gene cassette transcription prevents integrase expression in class 1 integrons. J Bacteriol 193 : 56755682.[PubMed] [CrossRef]
105. Vinué L,, Jové T,, Torres C,, Ploy MC . 2011. Diversity ofclass 1 integron gene cassette Pc promoter variants inclinical Escherichia coli strains and description of a new P2 promoter variant. Int J Antimicrob Agents 38 : 526529.[PubMed] [CrossRef]
106. Moura A,, Jové T,, Ploy MC,, Henriques I,, Correia A . 2012. Diversity of gene cassette promoters in class 1 integrons from wastewater environments. Appl Environ Microbiol 78 : 54135416.[PubMed] [CrossRef]
107. Bikard D,, Loot C,, Baharoglu Z,, Mazel D . 2010. Folded DNA in action: hairpin formation and biological functions in prokaryotes. Microbiol Mol BiolRev 74 : 570588.[PubMed] [CrossRef]
108. Trinh TQ,, Sinden RR . 1991. Preferential DNA secondary structure mutagenesis in the lagging strand of replication in E. coli . Nature 352 : 544547.[PubMed] [CrossRef]
109. Prudhomme M,, Attaiech L,, Sanchez G,, Martin B,, Claverys JP . 2006. Antibiotic stress induces genetic transformability in the human pathogen Streptococcus pneumoniae . Science 313 : 8992.[PubMed] [CrossRef]
110. Moore ME,, Lam A,, Bhatnagar S,, Solnick JV . 2014. Environmental determinants of transformation efficiency in Helicobacter pylori . J Bacteriol 196 : 337344.[PubMed] [CrossRef]
111. Pearson CE,, Zorbas H,, Price GB,, Zannis-Hadjopoulos M . 1996. Inverted repeats, stem-loops, and cruciforms: significance for initiation of DNA replication. J Cell Biochem 63 : 122.[PubMed] [CrossRef]
112. Lodge JK,, Kazic T,, Berg DE . 1989. Formation of supercoiling domains in plasmid pBR322. J Bacteriol 171 : 21812187.[PubMed]
113. Pruss GJ,, Drlica K . 1986. Topoisomerase I mutants: the gene on pBR322 that encodes resistance to tetracycline affects plasmid DNA supercoiling. Proc Natl Acad Sci USA 83 : 89528956.[PubMed] [CrossRef]
114. Liu LF,, Wang JC . 1987. Supercoiling of the DNA template during transcription. Proc Natl Acad Sci USA 84 : 70247027.[PubMed] [CrossRef]
115. Balke VL,, Gralla JD . 1987. Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli . J Bacteriol 169 : 44994506.[PubMed]
116. Jaworski A,, Higgins NP,, Wells RD,, Zacharias W . 1991. Topoisomerase mutants and physiological conditions control supercoiling and Z-DNA formation in vivo . J Biol Chem 266 : 25762581.[PubMed]
117. Ferrándiz MJ,, Martín-Galiano AJ,, Schvartzman JB,, de la Campa A . 2010. The genome of Streptococcus pneumoniae is organized in topology-reacting gene clusters. Nucleic Acids Res 38 : 35703581.[PubMed] [CrossRef]
118. Majchrzak M,, Bowater RP,, Staczek P,, Parniewski P . 2006. SOS repair and DNA supercoiling influence the genetic stability of DNA triplet repeats in Escherichia coli . J Mol Biol 364 : 612624.[PubMed] [CrossRef]
119. Champion K,, Higgins NP . 2007. Growth rate toxicity phenotypes and homeostatic supercoil control differentiate Escherichia coli from Salmonella enterica serovar Typhimurium . J Bacteriol 189 : 58395849.[PubMed] [CrossRef]
120. Collins J,, Volckaert G,, Nevers P . 1982. Precise and nearly-precise excision of the symmetrical inverted repeats of Tn5; common features of recA-independent deletion events in Escherichia coli . Gene 19 : 139146.[PubMed] [CrossRef]
121. Meyer RR,, Laine PS . 1990. The single-stranded DNA-binding protein of Escherichia coli . Microbiol Rev 54 : 342380.[PubMed]
122. Roy R,, Kozlov AG,, Lohman TM,, Ha T . 2009. SSB protein diffusion on single-stranded DNA stimulates RecA filament formation. Nature 461 : 10921097.[PubMed] [CrossRef]
123. Dubois V,, Debreyer C,, Quentin C,, Parissi V . 2009. In vitro recombination catalyzed by bacterial class 1 integron integrase IntI1 involves cooperative binding and specific oligomeric intermediates. PloS One 4 : e5228. [PubMed] [CrossRef]
124. Dubois V,, Debreyer C,, Litvak S,, Quentin C,, Parissi V . 2007. A new in vitro strand transfer assay for monitoring bacterial class 1 integron recombinase IntI1 activity. PLoS One 2 : e1315. [PubMed] [CrossRef]
125. Tanaka T,, Mizukoshi T,, Sasaki K,, Kohda D,, Masai H . 2007. Escherichia coli PriA protein, two modes of DNA binding and activation of ATP hydrolysis. J Biol Chem 282 : 1991719927.[PubMed] [CrossRef]
126. Grompone G,, Ehrlich SD,, Michel B . 2003. Replication restart in gyrB Escherichia coli mutants. Mol Microbiol 48 : 845854.[PubMed] [CrossRef]
127. Rowe-Magnus DA . 2009. Integrase-directed recovery of functional genes from genomic libraries. Nucleic Acids Res 37 : e118. [PubMed] [CrossRef]
128. Sureshan V,, Deshpande CN,, Boucher Y,, Koenig JE,, Midwest Center for Structural G, Stokes HW,, Harrop SJ,, Curmi PM,, Mabbutt BC . 2013. Integron gene cassettes: a repository of novel protein folds with distinct interaction sites. PloS One 8 : e52934. [PubMed] [CrossRef]
129. Gestal AM,, Liew EF,, Coleman NV . 2011. Natural transformation with synthetic gene cassettes: new tools for integron research and biotechnology. Microbiology 157 : 33493360.[PubMed] [CrossRef]
130. Bikard D,, Julié-Galau S,, Cambray G,, Mazel D . 2010. The synthetic integron: an in vivo genetic shuffling device. Nucleic Acids Res 38 : e153. [PubMed] [CrossRef]
131. Baquero F,, Coque TM,, de la Cruz F . 2011. Ecology and evolution as targets: the need for novel eco-evo drugs and strategies to fight antibiotic resistance. Antimicrob Agents Chemother 55 : 36493660.[PubMed] [CrossRef]
132. Holmes AJ,, Holley MP,, Mahon A,, Nield B,, Gillings M,, Stokes HW . 2003. Recombination activity of a distinctive integron-gene cassette system associated with Pseudomonas stutzeri populations in soil. J Bacteriol 185 : 918928.[PubMed] [CrossRef]
133. Leon G,, Roy PH . 2009. Potential role of group IIC-attC introns in integron cassette formation. J Bacteriol 191 : 60406051.[PubMed] [CrossRef]
134. Quiroga C,, Centrón D . 2009. Using genomic data to determine the diversity and distribution of target site motifs recognized by class C-attC group II introns. J Mol Evol 68 : 539549.[PubMed] [CrossRef]

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error