Class 1 integrons are low-cost structures in Escherichia coli

ISME Journal

Volumn 11, Issue 7, 2017, Pages 1535-1544

  Lacotte, Yohann ^a   Ploy, Marie Cécile ^a   Raherison, Sophie ^a  

^a UMR 1092   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBIOTIC RESISTANCE; BACTERIUM; ENZYME ACTIVITY; EXPERIMENTAL STUDY; FITNESS; GENE EXPRESSION; INHIBITION;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ANTIINFECTIVE AGENT; INTEGRASE;

CYTOLOGY; DRUG EFFECTS; ESCHERICHIA COLI; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; INTEGRON; PHYSIOLOGY; PROMOTER REGION; SOS RESPONSE (GENETICS);

ANTI-BACTERIAL AGENTS; BIOLOGICAL EVOLUTION; ESCHERICHIA COLI; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INTEGRASES; INTEGRONS; PROMOTER REGIONS, GENETIC; SOS RESPONSE (GENETICS);

EID: 85017132562     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2017.38     Document Type: Article

References (49)

1. Ahmed AM, Nakano H, Shimamoto T. (2005). Molecular characterization of integrons in non-typhoid Salmonella serovars isolated in Japan: description of an unusual class 2 integron. J Antimicrob Chemother 55: 371-374.
2. Avila P, de la Cruz F. (1988). Physical and genetic map of the IncW plasmid R388. Plasmid 20: 155-157.
3. Baharoglu Z, Mazel D. (2011). Vibrio cholerae triggers SOS and mutagenesis in response to a wide range of antibiotics: a route towards multiresistance. Antimicrob Agents Chemother 55: 2438-2441.
4. Barraud O, Ploy M-C. (2015). Diversity of class 1 integron gene cassette rearrangements selected under antibiotic pressure. J Bacteriol 197: 2171-2178.
5. Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D et al. (2004). Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol 51: 659-674.
6. Brolund A, Sundqvist M, Kahlmeter G, Grape M. (2010). Molecular characterisation of trimethoprim resistance in Escherichia coli and Klebsiella pneumoniae during a two year intervention on trimethoprim use. PLoS ONE 5: e9233.
7. Cambray G, Guerout, Mazel D. (2010). Integrons. Annu Rev Genet 44: 141-166.
8. Cambray G, Sanchez-Alberola N, Campoy S, Guerin É, Da Re S, González-Zorn B et al. (2011). Prevalence of SOS-mediated control of integron integrase expression as an adaptive trait of chromosomal and mobile integrons. Mob DNA 2: 6-6.
9. Chaveroche M-K, Ghigo J-M, d'Enfert C. (2000). A rapid method for efficient gene replacement in the filamentous fungus Aspergillus nidulans. Nucleic Acids Res 28: e97-e97.
10. Cherepanov PP, Wackernagel W. (1995). Gene disruption in Escherichia coli: TcR and KmR cassettes with the option of Flp-catalyzed excision of the antibioticresistance determinant. Gene 158: 9-14.
11. Collis CM, Hall RM. (1995). Expression of antibiotic resistance genes in the integrated cassettes of integrons. Antimicrob Agents Chemother 39: 155-162.
12. Engelstadter J, Harms K, Johnsen PJ. (2016). The evolutionary dynamics of integrons in changing environments. ISME J 10: 1296-1307.
13. Escudero JA, Loot C, Nivina A, Mazel D. (2015). The integron: adaptation on demand. Microbiol Spectr 3: MDNA3-0019-2014.
14. Escudero JA, Loot C, Parissi V, Nivina A, Bouchier C, Mazel D. (2016). Unmasking the ancestral activity of integron integrases reveals a smooth evolutionary transition during functional innovation. Nat Commun 7: 10937.
15. Espéli O, Moulin L, Boccard F. (2001). Transcription attenuation associated with bacterial repetitive extragenic BIME elements1. J Mol Biol 314: 375-386.
16. Foucault M-L, Depardieu F, Courvalin P, Grillot-Courvalin C. (2010). Inducible expression eliminates the fitness cost of vancomycin resistance in enterococci. Proc Natl Acad Sci USA 107: 16964-16969.
17. Gaze WH, Zhang L, Abdouslam NA, Hawkey PM, Calvo-Bado L, Royle J et al. (2011). Impacts of anthropogenic activity on the ecology of class 1 integrons and integron-associated genes in the environment. ISME J 5: 1253-1261.
18. Gillings MR, Holley MP, Stokes HW, Holmes AJ. (2005). Integrons in Xanthomonas: A source of species genome diversity. Proc Natl Acad Sci USA 102: 4419-4424.
19. Guerin É, Cambray G, Sanchez-Alberola N, Campoy S, Erill I, Da Re S et al. (2009). The SOS Response Controls Integron Recombination. Science 324: 1034-1034.
20. Guerra B, Junker E, Schroeter A, Helmuth R, Guth BEC, Beutin L. (2006). Phenotypic and genotypic characterization of antimicrobial resistance in Escherichia coli O111 isolates. J Antimicrob Chemother 57: 1210-1214.
21. Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, Hughes D et al. (2011). Selection of resistant bacteria at very low antibiotic concentrations. PLoS Pathog 7: e1002158.
22. Guérin E, Jové T, Tabesse A, Mazel D, Ploy M-C. (2011). High-level gene cassette transcription prevents integrase expression in class 1 integrons. J Bacteriol 193: 5675-5682.
23. Hanau-Berçot B, Podglajen I, Casin I, Collatz E. (2002). An intrinsic control element for translational initiation in class 1 integrons. Mol Microbiol 44: 119-130.
24. Hare JM, Adhikari S, Lambert KV, Hare AE, Grice AN. (2012). The Acinetobacter regulatory UmuDAb protein cleaves in response to DNA damage with chimeric LexA/UmuD characteristics. FEMS Microbiol Lett 334: 57-65.
25. Jacquier H, Zaoui C, Sanson-le Pors M-J, Mazel D, Berçot B. (2009). Translation regulation of integrons gene cassette expression by the attC sites. Mol Microbiol 72: 1475-1486.
26. Jové T, Da Re S, Denis F, Mazel D, Ploy M-C. (2010). Inverse correlation between promoter strength and excision activity in class 1 integrons. PLoS Genet 6: e1000793.
27. Kheiri R, Akhtari L. (2016). Antimicrobial resistance and integron gene cassette arrays in commensal Escherichia coli from human and animal sources in IRI. Gut Pathog 8: 40.
28. Larouche A, Roy PH. (2011). Effect of attC structure on cassette excision by integron integrases. Mob DNA 2: 3-3.
29. Lenski RE, Rose MR, Simpson SC, Tadler SC. (1991). Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 138: 1315-1341.
30. Levy SB, Marshall B. (2004). Antibacterial resistance worldwide: causes, challenges and responses. Nat Med 10: S122-S129.
31. 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: 762-771.
32. Lutz R, Bujard H. (1997). Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25: 1203-1210.
33. Mazel D. (2006). Integrons: agents of bacterial evolution. Nat Rev Microbiol 4: 608-620.
34. 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: 1-12.
35. Nguyen TN, Phan QG, Duong LP, Bertrand KP, Lenski RE. (1989). Effects of carriage and expression of the Tn10 tetracycline-resistance operon on the fitness of Escherichia coli K12. Mol Biol Evol 6: 213-225.
36. Payie KG, Clarke AJ. (1997). Characterization of gentamicin 2'-N-acetyltransferase from Providencia stuartii: its use of peptidoglycan metabolites for acetylation of both aminoglycosides and peptidoglycan. J Bacteriol 179: 4106-4114.
37. Pérez-Valdespino A, Lazarini-Martínez A, Rivera-González AX, García-Hernández N, Curiel-Quesada E. (2016). Dynamics of a class 1 integron located on plasmid or chromosome in two Aeromonas spp. strains. Front Microbiol 7: 1556.
38. Rao AN, Barlow M, Clark LA, Boring JR, Tenover FC, McGowan JE. (2006). Class 1 integrons in resistant Escherichia coli and Klebsiella spp., US hospitals. Emerg Infect Dis 12: 1011-1014.
39. Recchia GD, Stokes HW, Hall RM. (1994). Characterisation of specific and secondary recombination sites recognised by the integron DNA integrase. Nucleic Acids Res 22: 2071-2078.
40. Rodríguez-Verdugo A, Gaut BS, Tenaillon O. (2013). Evolution of Escherichia coli rifampicin resistance in an antibiotic-free environment during thermal stress. BMC Evol Biol 13: 1-11.
41. Schrag SJ, Perrot V, Levin BR. (1997). Adaptation to the fitness costs of antibiotic resistance in Escherichia coli. Proc R Soc B Biol Sci 264: 1287-1291.
42. Starikova I, Harms K, Haugen P, Lunde TTM, Primicerio R, Samuelsen Ø et al. (2012). A trade-off between the fitness cost of functional integrases and long-term stability of integrons. PLoS Pathog 8: e1003043.
43. Stokes HW, Hall RM. (1989). A novel family of potentially mobile DNA elements encoding site-specific gene-integration functions: integrons. Mol Microbiol 3: 1669-1683.
44. Subbiah M, Top EM, Shah DH, Call DR. (2011). Selection pressure required for long-term persistence of blaCMY- -2-positive IncA/C Ppasmids. Appl Environ Microbiol 77: 4486-4493.
45. Vasilakopoulou A, Psichogiou M, Tzouvelekis L, Tassios PT, Kosmidis C, Petrikkos G et al. (2009). Prevalence and characterization of class 1 integrons in Escherichia coli of poultry and human origin. Foodborne Pathog Dis 6: 1211-1218.
46. Vinué L, Jové T, Torres C, Ploy M-C. (2011). Diversity of class 1 integron gene cassette Pc promoter variants in clinical Escherichia coli strains and description of a new P2 promoter variant. Int J Antimicrob Agents 38: 526-529.
47. Vogwill T, MacLean RC. (2015). The genetic basis of the fitness costs of antimicrobial resistance: a metaanalysis approach. Evol Appl 8: 284-295.
48. Wei Q, Jiang X, Li M, Li G, Hu Q, Lu H et al. (2013). Diversity of gene Cassette promoter variants of class 1 integrons in uropathogenic Escherichia coli. Curr Microbiol 67: 543-549.
49. Wright MS, Baker-Austin C, Lindell AH, Stepanauskas R, Stokes HW, McArthur JV. (2008). Influence of industrial contamination on mobile genetic elements: class 1 integron abundance and gene cassette structure in aquatic bacterial communities. ISME J 2: 417-428.