DNA-Damaging Agents Induce the RecA-Independent Homologous Recombination Functions of Integrating Conjugative Elements of the SXT/R391 Family

Garriss, Geneviève; Poulin-Laprade, Dominic; Burrus, Vincent

doi:10.1128/jb.02090-12

Cited by 30 publications

(40 citation statements)

References 63 publications

(75 reference statements)

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“…1, blue arrows; Table 1). It also contained a regulatory region (eex, setCD, croS and setR), which can be activated upon DNA damage (Beaber et al, 2002;Garriss et al, 2013;Poulin-Laprade & Burrus, 2015) and a recombination system (bet/exo) responsible for generating hybrid forms . Moreover, sequence analysis of the entry exclusion gene, eex, confirmed that ICESh95 belongs to ICE exclusion group S (99 % nucleotide identity to eexS from ICE SXT MO10 ) (Marrero & Waldor, 2007).…”

Section: Genome Analysis Of the Clinical Strain Shewanella Sp Sh95mentioning

confidence: 99%

“…It has been reported that the bet/exo recombination system promotes the generation of hybrid versions of ICEs (Garriss et al, 2013. Thus, it is likely that the xis/int module was incorporated into the ICESh95 structure by a recombination event, which was probably mediated by its own Bet/ Exo system resulting in the generation of a novel ICE.…”

Section: Icesh95 Is a Hybrid Element Capable Of Selftransfermentioning

confidence: 99%

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Genome analysis of a clinical isolate of Shewanella sp. uncovered an active hybrid integrative and conjugative element carrying an integron platform inserted in a novel genomic locus

et al. 2016

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Shewanella spp. are currently considered to be emerging pathogens that can code for a bla OXA carbapenemase in their chromosome. Complete genome analysis of the clinical isolate Shewanella sp. Sh95 revealed that this strain is a novel species, which shares a lineage with marine isolates. Characterization of its resistome showed that it codes for genes drfA15, qacH and bla OXA-48. We propose that Shewanella sp. Sh95 acts as reservoir of bla . Moreover, analysis of mobilome showed that it contains a novel integrative and conjugative element (ICE), named ICESh95. Comparative analysis between the close relatives ICESpuPO1 from Shewanella sp. W3-18-1 and ICE SXT MO10 from Vibrio cholerae showed that ICESh95 encompassed two new regions, a type III restriction modification system and a multidrug resistance integron. The integron platform contained a novel arrangement formed by gene cassettes drfA15 and qacH, and a class C-attC group II intron. Furthermore, insertion of ICESh95 occurred at a unique target site, which correlated with the presence of a different xis/ int module. Mobility of ICESh95 was assessed and demonstrated its ability to self-transfer with high efficiency to different species of bacteria. Our results show that ICESh95 is a selftransmissible, mobile element, which can contribute to the dissemination of antimicrobial resistance; this is clearly a threat when natural bacteria from water ecosystems, such as Shewanella, act as vectors in its propagation.

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Section: Genome Analysis Of the Clinical Strain Shewanella Sp Sh95mentioning

confidence: 99%

Section: Icesh95 Is a Hybrid Element Capable Of Selftransfermentioning

confidence: 99%

Genome analysis of a clinical isolate of Shewanella sp. uncovered an active hybrid integrative and conjugative element carrying an integron platform inserted in a novel genomic locus

et al. 2016

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“…Both RecA and Bet/Exo act synergistically to promote hybrid ICE formation from ICE tandem arrays (63). Since bet and exo are part of a SetCD-activated operon, their activity promotes ICE plasticity in response to DNA damages (63,64).…”

Section: Evolution and Plasticitymentioning

confidence: 99%

“…In E. coli FlhC associates with FlhD in an FlhD 2 C 2 heterotetrameric complex that induces the transcription of genes involved in the biogenesis of cell surface flagella to mediate bacterial cell motility. SetC and SetD are thought to assemble in a similar complex to activate the ASMscience.org/MicrobiolSpectrumexpression of various genes or groups of genes in SXT, including traLEKBVA and traFHG, the int and xis genes, the mosAT toxin-antitoxin system, and the bet/ exo RecA-independent homologous recombination system (47,56,58,63,64,65). Interestingly, the SetCD transcriptional activator also targets genes that are located outside of SXT/R391 ICEs; it stimulates the expression of int MGI and triggers the expression of rdfM, two genes encoded by mobilizable genomic islands (MGIs) (see below) (66,67).…”

Section: Regulation Of Excision and Conjugative Transfermentioning

confidence: 99%

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

Carraro

Burrus

2014

Microbiol Spectr

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Integrative and Conjugative Elements (ICEs) are bacterial mobile genetic elements that play a key role in bacterial genomes dynamics and evolution. ICEs are widely distributed among virtually all bacterial genera. Recent extensive studies have unraveled their high diversity and complexity. The present review depicts the general conserved features of ICEs and describes more precisely three major families of ICEs that have been extensively studied in the past decade for their biology, their evolution and their impact on genomes dynamics. First, the large SXT/R391 family of ICEs disseminates antibiotic resistance genes and drives the exchange of mobilizable genomic islands (MGIs) between many enteric pathogens such as Vibrio cholerae. Second, ICEBs1 of Bacillus subtilis is the most well understood ICE of Gram-positive bacteria, notably regarding the regulation of its dissemination and its initially unforeseen extrachromosomal replication, which could be a common feature of ICEs of both Gram-positive and Gram-negative bacteria. Finally, ICESt1 and ICESt3 of Streptococcus thermophilus are the prototypes of a large family of ICEs widely distributed among various streptococci. These ICEs carry an original regulation module that associates regulators related to those of both SXT/R391 and ICEBs1. Study of ICESt1 and ICESt3 uncovered the cis-mobilization of related genomic islands (CIMEs) by a mechanism called accretion-mobilization, which likely represents a paradigm for the evolution of many ICEs and genomic islands. These three major families of ICEs give a glimpse about ICEs dynamics and their high impact on bacterial adaptation.

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“…The overlapping genes setC and setD encode the SetCD activator complex. SetCD was shown to bind upstream of the Ϫ35 sequence of 11 promoters in SXT/R391 ICEs, activating the expression of Ͼ40 genes essential for site-specific and homologous recombination, ICE replication and partition, and conjugative transfer (26)(27)(28). The functions of s082, s083, s084, and s086 remain unknown.…”

mentioning

confidence: 99%

A λ Cro-Like Repressor Is Essential for the Induction of Conjugative Transfer of SXT/R391 Elements in Response to DNA Damage

Poulin-Laprade

Burrus

2015

J Bacteriol

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Integrative and conjugative elements (ICEs) of the SXT/R391 family are the main contributors to acquired multidrug resistance in the seventh pandemic lineage of Vibrio cholerae, the etiological agent of the diarrheal disease cholera. Conjugative transfer of SXT/R391 ICEs is triggered by antibiotics and agents promoting DNA damage through RecA-dependent autoproteolysis of SetR, an ICE-encoded CI-like repressor. Here, we describe the role of CroS, a distant Cro homolog, as a key component contributing to the regulation of expression of the activator SetCD that orchestrates the expression of the conjugative transfer genes. We show that deletion of croS abolishes the SOS response-dependent induction of SXT despite the presence of a functional setR gene. Using quantitative reverse transcription-PCR and lacZ reporter assays, we also show that CroS represses setR and setCD expression by binding to operator sites shared with SetR. Furthermore, we provide evidence of an additional operator site bound by SetR and CroS. Finally, we show that SetCD expression generates a positive feedback loop due to SXT excision and replication in a fraction of the cell population. Together, these results refine our understanding of the genetic regulation governing the propagation of major vectors of multidrug resistance. IMPORTANCEHealthcare systems worldwide are challenged by an alarming drug resistance crisis caused by the massive and rapid propagation of antibiotic resistance genes and the associated emergence of multidrug-resistant pathogenic bacteria. SXT/R391 ICEs contribute to this phenomenon not only in clinical and environmental vibrios but also in several members of the family Enterobacteriaceae. We have identified and characterized here the regulator CroS as a key factor in the stimulation of conjugative transfer of these ICEs in response to DNA-damaging agents. We have also untangled conflicting evidence regarding autoactivation of transfer by the master activator of SXT/R391 ICEs, SetCD. Discovery of CroS provides a clearer and more complete understanding of the regulatory network that governs the dissemination of SXT/R391 ICEs in bacterial populations. Cholera is a severe infectious disease caused by the ingestion of food or water contaminated by Vibrio cholerae. This disease remains widespread in regions with limited access to clean water and where poor sanitation allows easy dissemination of the bacterium in drinking water sources. Cholera is characterized by a profuse watery diarrhea that rapidly induces massive fluid loss, causing severe dehydration of the patient, which may lead to death within 24 h of symptom onset. Although epidemic cholera is usually caused by V. cholerae O1, the unusual serogroup O139 emerged in the early 1990s as the cause of a cholera outbreak in India (1). O139 clinical isolates were found to be resistant to sulfamethoxazole and trimethoprim, two antibiotics commonly used for the treatment of severe cases of cholera (2). This resistance was found to be transmissible and linked to an integ...

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DNA-Damaging Agents Induce the RecA-Independent Homologous Recombination Functions of Integrating Conjugative Elements of the SXT/R391 Family

Cited by 30 publications

References 63 publications

Genome analysis of a clinical isolate of Shewanella sp. uncovered an active hybrid integrative and conjugative element carrying an integron platform inserted in a novel genomic locus

Genome analysis of a clinical isolate of Shewanella sp. uncovered an active hybrid integrative and conjugative element carrying an integron platform inserted in a novel genomic locus

Biology of Three ICE Families: SXT/R391, ICE Bs1 , and ICE St1 /ICE St3

A λ Cro-Like Repressor Is Essential for the Induction of Conjugative Transfer of SXT/R391 Elements in Response to DNA Damage

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