Abstract
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.
Highlights
Integrative and mobilizable elements (IMEs) are discrete, mobile chromosomal regions that can excise from the chromosome and borrow the mating apparatus of helper conjugative elements to transfer to a new bacterial host [1,2]
Using a comparative genomics approach based on genes conserved among members of the Salmonella Genomic Island 1 (SGI1) group, we identified diverse integrative elements distantly related to SGI1 in several species of Vibrio, Aeromonas, Salmonella, Pokkaliibacter, and Escherichia
We identified integrative elements distantly related to Salmonella Genomic Island 1 (SGI1), a key vector of antibiotic resistance genes in Gammaproteobacteria
Summary
Integrative and mobilizable elements (IMEs) are discrete, mobile chromosomal regions that can excise from the chromosome and borrow the mating apparatus of helper conjugative elements to transfer to a new bacterial host [1,2]. The site-specific recombination module contains genes and cis-acting sequences that mediate the integration of the IMEs into and their excision from the chromosome. The mobilization module includes the cis-acting origin of transfer (oriT) and usually encodes mobilization proteins required to initiate the conjugative transfer at oriT [1]. The excision of IMEs is elicited by conjugative plasmids or integrative and conjugative elements (ICEs). These helper elements encode the type IV secretion system (T4SS) that translocates the IME DNA into the recipient cell [1]
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