Abstract
The High Pathogenicity Island of Yersinia pseudotuberculosis IP32637 was previously shown to be horizontally transferable as part of a large chromosomal segment. We demonstrate here that at low temperature other chromosomal loci, as well as a non-mobilizable plasmid (pUC4K), are also transferable. This transfer, designated GDT4 (Generalized DNA Transfer at 4°C), required the presence of an IP32637 endogenous plasmid (pGDT4) that carries several mobile genetic elements and a conjugation machinery. We established that cure of this plasmid or inactivation of its sex pilus fully abrogates this process. Analysis of the mobilized pUC4K recovered from transconjugants revealed the insertion of one of the pGDT4–borne ISs, designated ISYps1, at different sites on the transferred plasmid molecules. This IS belongs to the IS6 family, which moves by replicative transposition, and thus could drive the formation of cointegrates between pGDT4 and the host chromosome and could mediate the transfer of chromosomal regions in an Hfr-like manner. In support of this model, we show that a suicide plasmid carrying ISYps1 is able to integrate itself, flanked by ISYps1 copies, at multiple locations into the Escherichia coli chromosome. Furthermore, we demonstrate the formation of RecA-independent cointegrates between the ISYps1-harboring plasmid and an ISYps1-free replicon, leading to the passive transfer of the non-conjugative plasmid. We thus demonstrate here a natural mechanism of horizontal gene exchange, which is less constrained and more powerful than the classical Hfr mechanism, as it only requires the presence of an IS6-type element on a conjugative replicon to drive the horizontal transfer of any large block of plasmid or chromosomal DNA. This natural mechanism of chromosome transfer, which occurs under conditions mimicking those found in the environment, may thus play a significant role in bacterial evolution, pathogenesis, and adaptation to new ecological niches.
Highlights
Horizontal gene transfer (HGT) is a driving force for bacterial evolution, as it allows the dispersion of adaptive loci between closely related and phylogenetically distant bacterial species
This phenomenon is not restricted to the High Pathogenicity Island (HPI) and to enterobacteria since it has been recently reported that movement of the Enterococcus faecalis pathogenicity islands (PAI) was invariably accompanied by transfer of flanking donor chromosome sequences [7]
Horizontal gene transfer is a major route for rapid bacterial evolution
Summary
Horizontal gene transfer (HGT) is a driving force for bacterial evolution, as it allows the dispersion of adaptive loci between closely related and phylogenetically distant bacterial species. The Gram-negative enteropathogen Yersinia pseudotuberculosis carries a PAI termed High Pathogenicity Island (HPI) [1], which encodes the siderophore yersiniabactin [2] The fact that this island is mobile within the genome of its host strain [3], and is present and often conserved both in terms of genetic organization and nucleotide sequence in various bacterial genera such as Escherichia coli (various pathotypes), Klebsiella or Citrobacter [4], suggested that it may have retained its ability to be horizontally transmitted to new bacterial hosts. We evidenced the transfer of the HPI between natural Y. pseudotuberculosis isolates [3] This phenomenon was observed only when the bacteria were incubated at low temperature (optimal at 4uC) and in broth, and was more efficient in an iron-poor medium [5]. This phenomenon is not restricted to the HPI and to enterobacteria since it has been recently reported that movement of the Enterococcus faecalis PAI was invariably accompanied by transfer of flanking donor chromosome sequences [7]
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