Genomic islands related to Salmonella genomic island 1; integrative mobilisable elements in trmE mobilised in trans by A/C plasmids

Curraize, Claire de; Siébor, Eliane; Neuwirth, Catherine

doi:10.1016/j.plasmid.2021.102565

Cited by 12 publications

(24 citation statements)

References 82 publications

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“…Since the initial report of SGI1 in Salmonella enterica serovar Typhimurium DT104 two decades ago, a multitude of SGI1 variants has been described in several species of Gammaproteobacteria , including human pathogens such as Salmonella enterica serovars, Proteus mirabilis , Morganella morganii , Providencia stuartii or Klebsiella pneumoniae ( 11–15 ). SGI1 and its variants share a conserved set of genes (described below) and often bear a class 1 integron with diverse combinations of antibiotic resistance gene cassettes ( 16 ). SGI1 and its relatives are found integrated at the 3′ end of trmE (also known as mnmE or thdF ) in the chromosome of their respective hosts and are specifically mobilised in trans by the IncC and closely related IncA conjugative plasmids ( 17 ).…”

Section: Introductionmentioning

confidence: 99%

Crucial role ofSalmonellagenomic island 1 master activator in the parasitism of IncC plasmids

Durand

Huguet

Rivard

et al. 2021

Nucleic Acids Research

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IncC conjugative plasmids and the multiple variants of Salmonella Genomic Island 1 (SGI1) are two functionally interacting families of mobile genetic elements commonly associated with multidrug resistance in the Gammaproteobacteria. SGI1 and its siblings are specifically mobilised in trans by IncC conjugative plasmids. Conjugative transfer of IncC plasmids is activated by the plasmid-encoded master activator AcaCD. SGI1 carries five AcaCD-responsive promoters that drive the expression of genes involved in its excision, replication, and mobilisation. SGI1 encodes an AcaCD homologue, the transcriptional activator complex SgaCD (also known as FlhDCSGI1) that seems to recognise and activate the same SGI1 promoters. Here, we investigated the relevance of SgaCD in SGI1′s lifecycle. Mating assays revealed the requirement for SgaCD and its IncC-encoded counterpart AcaCD in the mobilisation of SGI1. An integrative approach combining ChIP-exo, Cappable-seq, and RNA-seq confirmed that SgaCD activates each of the 18 AcaCD-responsive promoters driving the expression of the plasmid transfer functions. A comprehensive analysis of the activity of the complete set of AcaCD-responsive promoters of SGI1 and the helper IncC plasmid was performed through reporter assays. qPCR and flow cytometry assays revealed that SgaCD is essential to elicit the excision and replication of SGI1 and destabilise the helper IncC plasmid.

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Section: Introductionmentioning

confidence: 99%

Crucial role ofSalmonellagenomic island 1 master activator in the parasitism of IncC plasmids

Durand

Huguet

Rivard

et al. 2021

Nucleic Acids Research

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“…SGI1-like elements integrated at the 3' end of trmE are widespread in a broad range of Enterobacteriaceae and sporadically found in a few Vibrio species [12].…”

Section: Discussionmentioning

confidence: 99%

“…trmE encodes the 5-carboxymethylaminomethyluridine-tRNA synthase GTPase subunit. SGI1 variants have been reported in a wide array of Gammaproteobacteria, including Proteus mirabilis (PGI1), Acinetobacter baumannii (AGI1), Morganella, Providencia, Enterobacter, and Escherichia coli, but also in Vibrio cholerae and Klebsiella pneumoniae [10][11][12]. Most variants carry a class I integron structurally similar to the In104 integron of SGI1.…”

Section: Introductionmentioning

confidence: 99%

Genomic islands targeting dusA in Vibrio species are distantly related to Salmonella Genomic Island 1 and mobilizable by IncC conjugative plasmids

Durand

Deschênes

Burrus

2021

Preprint

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Salmonella Genomic Island 1 (SGI1) and its variants are significant contributors to the spread of antibiotic resistance among Gammaproteobacteria . All known SGI1 variants integrate at the 3’ end of trmE , a gene coding for a tRNA modification enzyme. SGI1 variants are mobilized specifically by conjugative plasmids of the incompatibility groups A and C (IncA and IncC). Using a comparative genomics approach based on genes conserved among members of the SGI1 group, we identified diverse genomic islands (GIs) distantly related to SGI1 in several species of Vibrio , Aeromonas , Salmonella , Pokkaliibacter , and Escherichia . Unlike SGI1, these GIs target two alternative chromosomal loci, the 5’ end of dusA and the 3’ end of yicC . Although these elements share many features with SGI1, they lack antibiotic resistance genes and carry alternative integration/excision modules. Functional characterization of MGI Vch USA3, a dusA -specific GI, revealed promoters that respond to AcaCD, the master activator of IncC plasmid transfer genes. Quantitative PCR and mating assays confirmed that MGI Vch USA3 excises from the chromosome and is mobilized by an IncC helper plasmid from Vibrio cholerae to Escherichia coli . MGI Vch USA3 encodes the AcaC homolog SgaC that associates with AcaD to form a hybrid activator complex AcaD/SgaC essential for its excision and mobilization. We identified the dusA -specific recombination directionality factor RdfN required for the integrase-mediated excision of dusA -specific GIs from the chromosome. Like xis in SGI1, rdfN is under the control of an AcaCD-responsive promoter. Although the integration of MGI Vch USA3 disrupts dusA , the GI provides a new promoter sequence and restores the reading frame of dusA for proper expression of the tRNA-dihydrouridine synthase A. Phylogenetic analysis of the conserved proteins encoded by SGI1-like elements targeting dusA , yicC , and trmE gives a fresh perspective on the possible origin of SGI1 and its variants.

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“…Salmonella Genomic Island 1 (SGI1) is certainly one of the most studied IMEs. Though first described 20 years ago, SGI1 and its siblings have only recently gained a lot of attention due to their prevalence and prominent role in the spread of multidrug resistance [ 7 , 8 ]. The canonical 43-kb SGI1 resides at the 3’ end of trmE (also known as mnmE or thdF ) in Salmonella enterica serovar Typhimurium DT104 [ 9 ].…”

Section: Introductionmentioning

confidence: 99%

“…trmE encodes the 5-carboxymethylaminomethyluridine-tRNA synthase GTPase subunit. SGI1 variants have been reported in a wide array of Gammaproteobacteria , including Proteus mirabilis (PGI1), Acinetobacter baumannii (AGI1), Morganella , Providencia , Enterobacter , Escherichia coli , Vibrio cholerae (GI-15), and Klebsiella pneumoniae [ 7 , 10 , 11 ]. Most variants carry a class I integron structurally similar to the In104 integron of SGI1.…”

Section: Introductionmentioning

confidence: 99%

Genomic islands targeting dusA in Vibrio species are distantly related to Salmonella Genomic Island 1 and mobilizable by IncC conjugative plasmids

2021

View full text Add to dashboard Cite

Salmonella Genomic Island 1 (SGI1) and its variants are significant contributors to the spread of antibiotic resistance among Gammaproteobacteria. All known SGI1 variants integrate at the 3’ end of trmE, a gene coding for a tRNA modification enzyme. SGI1 variants are mobilized specifically by conjugative plasmids of the incompatibility groups A and C (IncA and IncC). Using a comparative genomics approach based on genes conserved among members of the SGI1 group, we identified diverse integrative elements distantly related to SGI1 in several species of Vibrio, Aeromonas, Salmonella, Pokkaliibacter, and Escherichia. Unlike SGI1, these elements target two alternative chromosomal loci, the 5’ end of dusA and the 3’ end of yicC. Although they share many features with SGI1, they lack antibiotic resistance genes and carry alternative integration/excision modules. Functional characterization of IMEVchUSA3, a dusA-specific integrative element, revealed promoters that respond to AcaCD, the master activator of IncC plasmid transfer genes. Quantitative PCR and mating assays confirmed that IMEVchUSA3 excises from the chromosome and is mobilized by an IncC helper plasmid from Vibrio cholerae to Escherichia coli. IMEVchUSA3 encodes the AcaC homolog SgaC that associates with AcaD to form a hybrid activator complex AcaD/SgaC essential for its excision and mobilization. We identified the dusA-specific recombination directionality factor RdfN required for the integrase-mediated excision of dusA-specific elements from the chromosome. Like xis in SGI1, rdfN is under the control of an AcaCD-responsive promoter. Although the integration of IMEVchUSA3 disrupts dusA, it provides a new promoter sequence and restores the reading frame of dusA for proper expression of the tRNA-dihydrouridine synthase A. Phylogenetic analysis of the conserved proteins encoded by SGI1-like elements targeting dusA, yicC, and trmE gives a fresh perspective on the possible origin of SGI1 and its variants.

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Genomic islands related to Salmonella genomic island 1; integrative mobilisable elements in trmE mobilised in trans by A/C plasmids

Cited by 12 publications

References 82 publications

Crucial role ofSalmonellagenomic island 1 master activator in the parasitism of IncC plasmids

Crucial role ofSalmonellagenomic island 1 master activator in the parasitism of IncC plasmids

Genomic islands targeting dusA in Vibrio species are distantly related to Salmonella Genomic Island 1 and mobilizable by IncC conjugative plasmids

Genomic islands targeting dusA in Vibrio species are distantly related to Salmonella Genomic Island 1 and mobilizable by IncC conjugative plasmids

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