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Cited by 319Bacterial Genetics and BiotechnologyAntibiotic Resistance in BacteriaPharmaceutical and Antibiotic Environmental Impacts

Conjugative DNA Transfer Induces the Bacterial SOS Response and Promotes Antibiotic Resistance Development through Integron Activation

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Baharoglu, Zeynep, Bikard, David, Mazel, Didier·2010·PLoS Genetics
DOI 10.1371/journal.pgen.1001165PMC PMC2958807
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Abstract

Conjugation is one mechanism for intra- and inter-species horizontal gene transfer among bacteria. Conjugative elements have been instrumental in many bacterial species to face the threat of antibiotics, by allowing them to evolve and adapt to these hostile conditions. Conjugative plasmids are transferred to plasmidless recipient cells as single-stranded DNA. We used lacZ and gfp fusions to address whether conjugation induces the SOS response and the integron integrase. The SOS response controls a series of genes responsible for DNA damage repair, which can lead to recombination and mutagenesis. In this manuscript, we show that conjugative transfer of ssDNA induces the bacterial SOS stress response, unless an anti-SOS factor is present to alleviate this response. We also show that integron integrases are up-regulated during this process, resulting in increased cassette rearrangements. Moreover, the data we obtained using broad and narrow host range plasmids strongly suggests that plasmid transfer, even abortive, can trigger chromosomal gene rearrangements and transcriptional switches in the recipient cell. Our results highlight the importance of environments concentrating disparate bacterial communities as reactors for extensive genetic adaptation of bacteria.

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  • The accessory genome is more dynamic and may include genes acquired through mutation, recombination, horizontal gene transfer, plasmids, phages, transposons, or insertion sequences.

    “In contrast, the accessory genome is more dynamic and may include genes acquired through mutation, recombination, horizontal gene transfer, plasmids, phages, transposons, or insertion sequences. 27,28”

    From Comparative Genomic Insights into Pangenome Diversity and Functional Adaptation of Akkermansia and Faecalibacterium as Gut-Associated Next-Generation Probiotics: A Systematic Review (2026) · cites this paper as [28]

    The Introduction describes genome modification through mutation, rearrangement and horizontal gene transfer, while the Discussion links conjugative plasmid transfer to gene rearrangements. The paper does not characterize the accessory genome as more dynamic or support the full list of proposed sources, particularly phages, transposons and insertion sequences. The indexed passages have no page numbers. (LLM, conf=0.86)

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  • In bacterial populations, the core genome generally represents conserved functions.

    “In bacterial populations, the core genome generally represents conserved functions.”

    From Comparative Genomic Insights into Pangenome Diversity and Functional Adaptation of Akkermansia and Faecalibacterium as Gut-Associated Next-Generation Probiotics: A Systematic Review (2026) · cites this paper as [28]

    The Introduction discusses bacterial adaptation, gene regulation, and horizontal gene transfer, but does not describe a core genome or say that it represents conserved functions. Searches of our copy for “core genome conserved functions” and “conserved genes essential functions bacterial populations” found no passage addressing that claim. (LLM, conf=0.74)

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Research works printed but not linked: 60

  1. [1]Hammer BK Bassler BL 2003 Quorum sensing controls biofilm formation in Vibrio cholerae. Mol Microbiol 50 101 104 14507367
  2. [2]Zhu J Miller MB Vance RE Dziejman M Bassler BL 2002 Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A 99 3129 3134 11854465 PMC122484
  3. [3]Silva AJ Benitez JA 2004 Transcriptional regulation of Vibrio cholerae hemagglutinin/protease by the cyclic AMP receptor protein and RpoS. J Bacteriol 186 6374 6382 15375117 PMC516606
  4. [4]Barker MM Gaal T Gourse RL 2001 Mechanism of regulation of transcription initiation by ppGpp. II. Models for positive control based on properties of RNAP mutants and competition for RNAP. J Mol Biol 305 689 702 11162085
  5. [5]Barker MM Gaal T Josaitis CA Gourse RL 2001 Mechanism of regulation of transcription initiation by ppGpp. I. Effects of ppGpp on transcription initiation in vivo and in vitro. J Mol Biol 305 673 688 11162084
  6. [7]Vielmetter W Bonhoeffer F Schutte A 1968 Genetic evidence for transfer of a single DNA strand during bacterial conjugation. J Mol Biol 37 81 86 5760496
  7. [8]Bialkowska-Hobrzanska H Kunicki-Goldfinger JH 1977 Mechanism of conjugation and recombination in bacteria XVI: single-stranded regions in recipient deoxyribonucleic acid during conjugation in Escherichia coli K-12. Mol Gen Genet 151 319 326 325377
  8. [9]Golub E Bailone A Devoret R 1988 A gene encoding an SOS inhibitor is present in different conjugative plasmids. J Bacteriol 170 4392 4394 3045095 PMC211458
  9. [10]Jones AL Barth PT Wilkins BM 1992 Zygotic induction of plasmid ssb and psiB genes following conjugative transfer of Incl1 plasmid Collb-P9. Mol Microbiol 6 605 613 1552860
  10. [11]Althorpe NJ Chilley PM Thomas AT Brammar WJ Wilkins BM 1999 Transient transcriptional activation of the Incl1 plasmid anti-restriction gene (ardA) and SOS inhibition gene (psiB) early in conjugating recipient bacteria. Mol Microbiol 31 133 142 9987116
  11. [12]Masai H Arai K 1997 Frpo: a novel single-stranded DNA promoter for transcription and for primer RNA synthesis of DNA replication. Cell 89 897 907 9200608
  12. [13]Bagdasarian M D'Ari R Filipowicz W George J 1980 Suppression of induction of SOS functions in an Escherichia coli tif-1 mutant by plasmid R100.1. J Bacteriol 141 464 469 6444942 PMC293648
  13. [14]Bagdasarian M Bailone A Bagdasarian MM Manning PA Lurz R 1986 An inhibitor of SOS induction, specified by a plasmid locus in Escherichia coli. Proc Natl Acad Sci U S A 83 5723 5726 3526338 PMC386361
  14. [15]Dutreix M Backman A Celerier J Bagdasarian MM Sommer S 1988 Identification of psiB genes of plasmids F and R6-5. Molecular basis for psiB enhanced expression in plasmid R6-5. Nucleic Acids Res 16 10669 10679 3205720 PMC338932
  15. [16]Bagdasarian M Bailone A Angulo JF Scholz P Bagdasarian M 1992 PsiB, and anti-SOS protein, is transiently expressed by the F sex factor during its transmission to an Escherichia coli K-12 recipient. Mol Microbiol 6 885 893 1318487
  16. [17]Lester CH Frimodt-Moller N Hammerum AM 2004 Conjugal transfer of aminoglycoside and macrolide resistance between Enterococcus faecium isolates in the intestine of streptomycin-treated mice. FEMS Microbiol Lett 235 385 391 15183889
  17. [18]Kurokawa K Itoh T Kuwahara T Oshima K Toh H 2007 Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res 14 169 181 17916580 PMC2533590
  18. [19]Garcia-Quintanilla M Ramos-Morales F Casadesus J 2008 Conjugal transfer of the Salmonella enterica virulence plasmid in the mouse intestine. J Bacteriol 190 1922 1927 18178735 PMC2258861
  19. [20]Feld L Schjorring S Hammer K Licht TR Danielsen M 2008 Selective pressure affects transfer and establishment of a Lactobacillus plantarum resistance plasmid in the gastrointestinal environment. J Antimicrob Chemother 61 845 852 18238887
  20. [21]Trobos M Lester CH Olsen JE Frimodt-Moller N Hammerum AM 2009 Natural transfer of sulphonamide and ampicillin resistance between Escherichia coli residing in the human intestine. J Antimicrob Chemother 63 80 86 18957394
  21. [22]Nogueira T Rankin DJ Touchon M Taddei F Brown SP 2009 Horizontal gene transfer of the secretome drives the evolution of bacterial cooperation and virulence. Curr Biol 19 1683 1691 19800234 PMC2773837
  22. [23]de la Cruz F Davies J 2000 Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol 8 128 133 10707066
  23. [24]Mazel D 2006 Integrons: agents of bacterial evolution. Nat Rev Microbiol 4 608 620 16845431
  24. [25]Rowe-Magnus DA Mazel D 1999 Resistance gene capture. Curr Opin Microbiol 2 483 488 10508722
  25. [26]Martinez-Freijo P Fluit AC Schmitz FJ Grek VS Verhoef J 1998 Class I integrons in Gram-negative isolates from different European hospitals and association with decreased susceptibility to multiple antibiotic compounds. J Antimicrob Chemother 42 689 696 10052890
  26. [27]Collis CM Kim MJ Stokes HW Hall RM 1998 Binding of the purified integron DNA integrase Intl1 to integron- and cassette-associated recombination sites. Mol Microbiol 29 477 490 9720866
  27. [28]Bouvier M Demarre G Mazel D 2005 Integron cassette insertion: a recombination process involving a folded single strand substrate. Embo J 24 4356 4367 16341091 PMC1356339
  28. [29]Jove 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 doi: 10.1371/journal.pgen.1000793 20066027 PMC2791841 · DOI
  29. [30]Rowe-Magnus DA Mazel D 2002 The role of integrons in antibiotic resistance gene capture. Int J Med Microbiol 292 115 125 12195734
  30. [31]Guerin E Cambray G Sanchez-Alberola N Campoy S Erill I 2009 The SOS response controls integron recombination. Science 324 1034 19460999
  31. [32]Couturier M Bex F Bergquist PL Maas WK 1988 Identification and classification of bacterial plasmids. Microbiol Rev 52 375 395 3054468 PMC373151
  32. [33]Eckerson HW Reynard AM 1977 Effect of entry exclusion on mating aggregates and transconjugants. J Bacteriol 129 131 137 318636 PMC234905
  33. [34]Garcillan-Barcia MP de la Cruz F 2008 Why is entry exclusion an essential feature of conjugative plasmids? Plasmid 60 1 18 18440635
  34. [35]Garriss G Waldor MK Burrus V 2009 Mobile antibiotic resistance encoding elements promote their own diversity. PLoS Genet 5 e1000775 doi: 10.1371/journal.pgen.1000775 20019796 PMC2786100 · DOI
  35. [36]Wozniak RA Fouts DE Spagnoletti M Colombo MM Ceccarelli D 2009 Comparative ICE genomics: insights into the evolution of the SXT/R391 family of ICEs. PLoS Genet 5 e1000786 doi: 10.1371/journal.pgen.1000786 20041216 PMC2791158 · DOI
  36. [37]Beaber JW Hochhut B Waldor MK 2004 SOS response promotes horizontal dissemination of antibiotic resistance genes. Nature 427 72 74 14688795
  37. [38]Burrus V Waldor MK 2003 Control of SXT integration and excision. J Bacteriol 185 5045 5054 12923077 PMC181012
  38. [39]Howland CJ Rees CE Barth PT Wilkins BM 1989 The ssb gene of plasmid ColIb-P9. J Bacteriol 171 2466 2473 2651402 PMC209922
  39. [40]Delver EP Belogurov AA 1997 Organization of the leading region of IncN plasmid pKM101 (R46): a regulation controlled by CUP sequence elements. J Mol Biol 271 13 30 9300052
  40. [41]Komano T Yoshida T Narahara K Furuya N 2000 The transfer region of IncI1 plasmid R64: similarities between R64 tra and legionella icm/dot genes. Mol Microbiol 35 1348 1359 10760136
  41. [42]Chilley PM Wilkins BM 1995 Distribution of the ardA family of antirestriction genes on conjugative plasmids. Microbiology 141 Pt 9 2157 2164 7496527
  42. [43]Petrova V Chitteni-Pattu S Drees JC Inman RB Cox MM 2009 An SOS Inhibitor that Binds to Free RecA Protein: The PsiB Protein. Mol Cell 36 121 130 19818715 PMC2761248
  43. [44]Rowe-Magnus DA Guerout AM Mazel D 2002 Bacterial resistance evolution by recruitment of super-integron gene cassettes. Mol Microbiol 43 1657 1669 11952913
  44. [45]Biskri L Bouvier M Guerout AM Boisnard S Mazel D 2005 Comparative study of class 1 integron and Vibrio cholerae superintegron integrase activities. J Bacteriol 187 1740 1750 15716446 PMC1063995
  45. [46]Matic I Rayssiguier C Radman M 1995 Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell 80 507 515 7859291
  46. [47]Matic I Taddei F Radman M 2000 No genetic barriers between Salmonella enterica serovar typhimurium and Escherichia coli in SOS-induced mismatch repair-deficient cells. J Bacteriol 182 5922 5924 11004198 PMC94721
  47. [48]Delmas S Matic I 2005 Cellular response to horizontally transferred DNA in Escherichia coli is tuned by DNA repair systems. DNA Repair (Amst) 4 221 229 15590330
  48. [49]Furuya N Komano T 1994 Surface exclusion gene of IncI1 plasmid R64: nucleotide sequence and analysis of deletion mutants. Plasmid 32 80 84 7991676
  49. [50]Kelley WL 2006 Lex marks the spot: the virulent side of SOS and a closer look at the LexA regulon. Mol Microbiol 62 1228 1238 17042786
  50. [51]Revilla C Garcillan-Barcia MP Fernandez-Lopez R Thomson NR Sanders M 2008 Different pathways to acquiring resistance genes illustrated by the recent evolution of IncW plasmids. Antimicrob Agents Chemother 52 1472 1480 18268088 PMC2292564
  51. [52]Komano T 1999 Shufflons: multiple inversion systems and integrons. Annu Rev Genet 33 171 191 10690407
  52. [53]Molin S Tolker-Nielsen T 2003 Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 14 255 261 12849777
  53. [54]Wuertz S Okabe S Hausner M 2004 Microbial communities and their interactions in biofilm systems: an overview. Water Sci Technol 49 327 336 15303758
  54. [55]Sorensen SJ Bailey M Hansen LH Kroer N Wuertz S 2005 Studying plasmid horizontal transfer in situ: a critical review. Nat Rev Microbiol 3 700 710 16138098
  55. [56]Huq A Whitehouse CA Grim CJ Alam M Colwell RR 2008 Biofilms in water, its role and impact in human disease transmission. Curr Opin Biotechnol 19 244 247 18524568
  56. [57]Perez-Mendoza D de la Cruz F 2009 Escherichia coli genes affecting recipient ability in plasmid conjugation: are there any? BMC Genomics 10 71 19203375 PMC2645431
  57. [58]Hao W Golding GB 2009 Does gene translocation accelerate the evolution of laterally transferred genes? Genetics 182 1365 1375 19474197 PMC2728873
  58. [59]Dimpfl J Echols H 1989 Duplication mutation as an SOS response in Escherichia coli: enhanced duplication formation by a constitutively activated RecA. Genetics 123 255 260 2684744 PMC1203797
  59. [60]Meibom KL Blokesch M Dolganov NA Wu CY Schoolnik GK 2005 Chitin induces natural competence in Vibrio cholerae. Science 310 1824 1827 16357262
  60. [61]Miller 1992 A short course in bacterial genetics Cold Spring Harbor, NY Cold Spring Harbor Laboratory Press

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Authors
Baharoglu, Z., Bikard, D., & Mazel, D.
Affiliations
Centre National de la Recherche Scientifique (FR)
Corresponding author
Mazel, Didier
ORCID
Venue
PLoS Genetics
Publisher
Public Library of Science (PLoS)
Published
2010-10-21
Volume
6
Issue
10
Pages
e1001165
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1001165
PMC
PMC2958807
OpenAlex
W2047606370
Cited by
319
References
0
Citations by year
2026: 27 · 2025: 26 · 2024: 30 · 2023: 29 · 2022: 27 · 2021: 31 · 2020: 14 · 2019: 17 · 2018: 17 · 2017: 15 · 2016: 11 · 2015: 12 · 2014: 13 · 2013: 22 · 2012: 12
FWCI
8.46
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
Funders
  • Agence Nationale de la Recherche (ANR-08-MIE-016, ANR-08-MIEN-0016)
  • Centre National de la Recherche Scientifique
  • Cilag
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Medicine › Antibiotic Resistance in Bacteria
  • Physical Sciences › Environmental Science › Pollution › Pharmaceutical and Antibiotic Environmental Impacts
Keywords
conjugative transfer, SOS response, integron integrase, antibiotic resistance, horizontal gene transfer, conjugative plasmids, single-stranded DNA, transcriptional switching, DNA repair
MeSH terms
Adaptation, Physiological, Bacteria, Conjugation, Genetic, DNA, Single-Stranded, Drug Resistance, Microbial, Escherichia coli, Lac Operon, Plasmids, Recombinant Fusion Proteins, SOS Response, Genetics, Time Factors, Vibrio cholerae, Gene Expression Regulation, Bacterial, Integrases, Gene Transfer, Horizontal, Integrons, Green Fluorescent Proteins

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