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Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli

Bacteria undergo horizontal gene transfer via various mechanisms. We recently reported that cell-to-cell transfer of nonconjugative plasmids occurs between strains of Escherichia coli in co-cultures, and that a specific strain (CAG18439) causes frequent plasmid transfer involving a DNase-sensitive m...

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Autores principales: Sugiura, Chiaki, Miyaue, Saki, Shibata, Yuka, Matsumoto, Akiko, Maeda, Sumio
Formato: Online Artículo Texto
Lenguaje:English
Publicado: AIMS Press 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6604958/
https://www.ncbi.nlm.nih.gov/pubmed/31294189
http://dx.doi.org/10.3934/microbiol.2017.4.784
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author Sugiura, Chiaki
Miyaue, Saki
Shibata, Yuka
Matsumoto, Akiko
Maeda, Sumio
author_facet Sugiura, Chiaki
Miyaue, Saki
Shibata, Yuka
Matsumoto, Akiko
Maeda, Sumio
author_sort Sugiura, Chiaki
collection PubMed
description Bacteria undergo horizontal gene transfer via various mechanisms. We recently reported that cell-to-cell transfer of nonconjugative plasmids occurs between strains of Escherichia coli in co-cultures, and that a specific strain (CAG18439) causes frequent plasmid transfer involving a DNase-sensitive mechanism, which we termed “cell-to-cell transformation”. Here we found that CAG18439 is a type of P1 bacteriophage lysogen that continuously releases phages. We tested the ability of P1vir bacteriophage to induce horizontal plasmid transfer and demonstrated that such a horizontal plasmid transfer was caused by adding culture supernatants of P1vir-infected cells harboring plasmids to other plasmid-free cells. This plasmid transfer system also reproduced the major features of plasmid transfer involving CAG18439, suggesting that P1vir-induced plasmid transfer is equivalent or very similar to plasmid transfer involving CAG18439. We further revealed that approximately two-thirds of the P1vir-induced plasmid transfer was DNase-sensitive, but that complete abolition of plasmid transfer was observed when proteins were denatured or removed, despite the presence or absence of DNase. Therefore, we concluded that P1vir-induced plasmid transfer is largely due to the occurrence of cell-to-cell transformation, which involves the assistance of some proteinaceous factor, and partly due to the occurrence of plasmid transduction, which is mediated by phage virions. This is the first demonstration of the P1-phage-induced cell-to-cell transformation.
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spelling pubmed-66049582019-07-10 Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli Sugiura, Chiaki Miyaue, Saki Shibata, Yuka Matsumoto, Akiko Maeda, Sumio AIMS Microbiol Research Article Bacteria undergo horizontal gene transfer via various mechanisms. We recently reported that cell-to-cell transfer of nonconjugative plasmids occurs between strains of Escherichia coli in co-cultures, and that a specific strain (CAG18439) causes frequent plasmid transfer involving a DNase-sensitive mechanism, which we termed “cell-to-cell transformation”. Here we found that CAG18439 is a type of P1 bacteriophage lysogen that continuously releases phages. We tested the ability of P1vir bacteriophage to induce horizontal plasmid transfer and demonstrated that such a horizontal plasmid transfer was caused by adding culture supernatants of P1vir-infected cells harboring plasmids to other plasmid-free cells. This plasmid transfer system also reproduced the major features of plasmid transfer involving CAG18439, suggesting that P1vir-induced plasmid transfer is equivalent or very similar to plasmid transfer involving CAG18439. We further revealed that approximately two-thirds of the P1vir-induced plasmid transfer was DNase-sensitive, but that complete abolition of plasmid transfer was observed when proteins were denatured or removed, despite the presence or absence of DNase. Therefore, we concluded that P1vir-induced plasmid transfer is largely due to the occurrence of cell-to-cell transformation, which involves the assistance of some proteinaceous factor, and partly due to the occurrence of plasmid transduction, which is mediated by phage virions. This is the first demonstration of the P1-phage-induced cell-to-cell transformation. AIMS Press 2017-10-10 /pmc/articles/PMC6604958/ /pubmed/31294189 http://dx.doi.org/10.3934/microbiol.2017.4.784 Text en © 2017 Sumio Maeda, et al., licensee AIMS Press This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0)
spellingShingle Research Article
Sugiura, Chiaki
Miyaue, Saki
Shibata, Yuka
Matsumoto, Akiko
Maeda, Sumio
Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli
title Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli
title_full Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli
title_fullStr Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli
title_full_unstemmed Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli
title_short Bacteriophage P1vir-induced cell-to-cell plasmid transformation in Escherichia coli
title_sort bacteriophage p1vir-induced cell-to-cell plasmid transformation in escherichia coli
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6604958/
https://www.ncbi.nlm.nih.gov/pubmed/31294189
http://dx.doi.org/10.3934/microbiol.2017.4.784
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