A natural system of chromosome transfer in Yersinia pseudotuberculosis.

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. T...

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Main Authors: Biliana Lesic, Mohamed Zouine, Magaly Ducos-Galand, Christèle Huon, Marie-Laure Rosso, Marie-Christine Prévost, Didier Mazel, Elisabeth Carniel
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2012-01-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3297565?pdf=render
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spelling doaj-cd41bbe82f4c412bac42e7494e08434d2020-11-25T02:12:46ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042012-01-0183e100252910.1371/journal.pgen.1002529A natural system of chromosome transfer in Yersinia pseudotuberculosis.Biliana LesicMohamed ZouineMagaly Ducos-GalandChristèle HuonMarie-Laure RossoMarie-Christine PrévostDidier MazelElisabeth CarnielThe 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.http://europepmc.org/articles/PMC3297565?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Biliana Lesic
Mohamed Zouine
Magaly Ducos-Galand
Christèle Huon
Marie-Laure Rosso
Marie-Christine Prévost
Didier Mazel
Elisabeth Carniel
spellingShingle Biliana Lesic
Mohamed Zouine
Magaly Ducos-Galand
Christèle Huon
Marie-Laure Rosso
Marie-Christine Prévost
Didier Mazel
Elisabeth Carniel
A natural system of chromosome transfer in Yersinia pseudotuberculosis.
PLoS Genetics
author_facet Biliana Lesic
Mohamed Zouine
Magaly Ducos-Galand
Christèle Huon
Marie-Laure Rosso
Marie-Christine Prévost
Didier Mazel
Elisabeth Carniel
author_sort Biliana Lesic
title A natural system of chromosome transfer in Yersinia pseudotuberculosis.
title_short A natural system of chromosome transfer in Yersinia pseudotuberculosis.
title_full A natural system of chromosome transfer in Yersinia pseudotuberculosis.
title_fullStr A natural system of chromosome transfer in Yersinia pseudotuberculosis.
title_full_unstemmed A natural system of chromosome transfer in Yersinia pseudotuberculosis.
title_sort natural system of chromosome transfer in yersinia pseudotuberculosis.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2012-01-01
description 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.
url http://europepmc.org/articles/PMC3297565?pdf=render
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