IS-linked movement of a restriction-modification system.

Potential mobility of restriction-modification systems has been suggested by evolutionary/bioinformatic analysis of prokaryotic genomes. Here we demonstrate in vivo movement of a restriction-modification system within a genome under a laboratory condition. After blocking replication of a temperature...

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Main Authors: Noriko Takahashi, Seishi Ohashi, Marat R Sadykov, Yoko Mizutani-Ui, Ichizo Kobayashi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-01-01
Series:PLoS ONE
Online Access:http://europepmc.org/articles/PMC3031569?pdf=render
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author Noriko Takahashi
Seishi Ohashi
Marat R Sadykov
Yoko Mizutani-Ui
Ichizo Kobayashi
author_facet Noriko Takahashi
Seishi Ohashi
Marat R Sadykov
Yoko Mizutani-Ui
Ichizo Kobayashi
author_sort Noriko Takahashi
collection DOAJ
description Potential mobility of restriction-modification systems has been suggested by evolutionary/bioinformatic analysis of prokaryotic genomes. Here we demonstrate in vivo movement of a restriction-modification system within a genome under a laboratory condition. After blocking replication of a temperature-sensitive plasmid carrying a PaeR7I restriction-modification system in Escherichia coli cells, the plasmid was found integrated into the chromosome of the surviving cells. Sequence analysis revealed that, in the majority of products, the restriction-modification system was linked to chromosomal insertion sequences (ISs). Three types of products were: (I) apparent co-integration of the plasmid and the chromosome at a chromosomal IS1 or IS5 copy (24/28 analyzed); (II) de novo insertion of IS1 with the entire plasmid except for a 1-3 bp terminal deletion (2/28); and (III) reciprocal crossing-over between the plasmid and the chromosome involving 1-3 bp of sequence identity (2/28). An R-negative mutation apparently decreased the efficiency of successful integration by two orders of magnitude. Reconstruction experiments demonstrated that the restriction-dependence was mainly due to selection against cells without proper integration: their growth was inhibited by the restriction enzyme action. These results demonstrate collaboration of a mobile element and a restriction-modification system for successful joint migration. This collaboration may have promoted the spread and, therefore, the long-term persistence of these complexes and restriction-modification systems in a wide range of prokaryotes.
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spelling doaj.art-35ea1e560a774bf3a29f9073f255bdc12022-12-22T02:00:10ZengPublic Library of Science (PLoS)PLoS ONE1932-62032011-01-0161e1655410.1371/journal.pone.0016554IS-linked movement of a restriction-modification system.Noriko TakahashiSeishi OhashiMarat R SadykovYoko Mizutani-UiIchizo KobayashiPotential mobility of restriction-modification systems has been suggested by evolutionary/bioinformatic analysis of prokaryotic genomes. Here we demonstrate in vivo movement of a restriction-modification system within a genome under a laboratory condition. After blocking replication of a temperature-sensitive plasmid carrying a PaeR7I restriction-modification system in Escherichia coli cells, the plasmid was found integrated into the chromosome of the surviving cells. Sequence analysis revealed that, in the majority of products, the restriction-modification system was linked to chromosomal insertion sequences (ISs). Three types of products were: (I) apparent co-integration of the plasmid and the chromosome at a chromosomal IS1 or IS5 copy (24/28 analyzed); (II) de novo insertion of IS1 with the entire plasmid except for a 1-3 bp terminal deletion (2/28); and (III) reciprocal crossing-over between the plasmid and the chromosome involving 1-3 bp of sequence identity (2/28). An R-negative mutation apparently decreased the efficiency of successful integration by two orders of magnitude. Reconstruction experiments demonstrated that the restriction-dependence was mainly due to selection against cells without proper integration: their growth was inhibited by the restriction enzyme action. These results demonstrate collaboration of a mobile element and a restriction-modification system for successful joint migration. This collaboration may have promoted the spread and, therefore, the long-term persistence of these complexes and restriction-modification systems in a wide range of prokaryotes.http://europepmc.org/articles/PMC3031569?pdf=render
spellingShingle Noriko Takahashi
Seishi Ohashi
Marat R Sadykov
Yoko Mizutani-Ui
Ichizo Kobayashi
IS-linked movement of a restriction-modification system.
PLoS ONE
title IS-linked movement of a restriction-modification system.
title_full IS-linked movement of a restriction-modification system.
title_fullStr IS-linked movement of a restriction-modification system.
title_full_unstemmed IS-linked movement of a restriction-modification system.
title_short IS-linked movement of a restriction-modification system.
title_sort is linked movement of a restriction modification system
url http://europepmc.org/articles/PMC3031569?pdf=render
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