Tight regulation of the intS gene of the KplE1 prophage: a new paradigm for integrase gene regulation.

Temperate phages have the ability to maintain their genome in their host, a process called lysogeny. For most, passive replication of the phage genome relies on integration into the host's chromosome and becoming a prophage. Prophages remain silent in the absence of stress and replicate passive...

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Main Authors: Gaël Panis, Yohann Duverger, Elise Courvoisier-Dezord, Stéphanie Champ, Emmanuel Talla, Mireille Ansaldi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2010-10-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC2951348?pdf=render
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author Gaël Panis
Yohann Duverger
Elise Courvoisier-Dezord
Stéphanie Champ
Emmanuel Talla
Mireille Ansaldi
author_facet Gaël Panis
Yohann Duverger
Elise Courvoisier-Dezord
Stéphanie Champ
Emmanuel Talla
Mireille Ansaldi
author_sort Gaël Panis
collection DOAJ
description Temperate phages have the ability to maintain their genome in their host, a process called lysogeny. For most, passive replication of the phage genome relies on integration into the host's chromosome and becoming a prophage. Prophages remain silent in the absence of stress and replicate passively within their host genome. However, when stressful conditions occur, a prophage excises itself and resumes the viral cycle. Integration and excision of phage genomes are mediated by regulated site-specific recombination catalyzed by tyrosine and serine recombinases. In the KplE1 prophage, site-specific recombination is mediated by the IntS integrase and the TorI recombination directionality factor (RDF). We previously described a sub-family of temperate phages that is characterized by an unusual organization of the recombination module. Consequently, the attL recombination region overlaps with the integrase promoter, and the integrase and RDF genes do not share a common activated promoter upon lytic induction as in the lambda prophage. In this study, we show that the intS gene is tightly regulated by its own product as well as by the TorI RDF protein. In silico analysis revealed that overlap of the attL region with the integrase promoter is widely encountered in prophages present in prokaryotic genomes, suggesting a general occurrence of negatively autoregulated integrase genes. The prediction that these integrase genes are negatively autoregulated was biologically assessed by studying the regulation of several integrase genes from two different Escherichia coli strains. Our results suggest that the majority of tRNA-associated integrase genes in prokaryotic genomes could be autoregulated and that this might be correlated with the recombination efficiency as in KplE1. The consequences of this unprecedented regulation for excessive recombination are discussed.
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spelling doaj.art-fe6e1dd67c094ed1bdae308b2e950abf2022-12-21T18:41:27ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042010-10-0161010.1371/journal.pgen.1001149Tight regulation of the intS gene of the KplE1 prophage: a new paradigm for integrase gene regulation.Gaël PanisYohann DuvergerElise Courvoisier-DezordStéphanie ChampEmmanuel TallaMireille AnsaldiTemperate phages have the ability to maintain their genome in their host, a process called lysogeny. For most, passive replication of the phage genome relies on integration into the host's chromosome and becoming a prophage. Prophages remain silent in the absence of stress and replicate passively within their host genome. However, when stressful conditions occur, a prophage excises itself and resumes the viral cycle. Integration and excision of phage genomes are mediated by regulated site-specific recombination catalyzed by tyrosine and serine recombinases. In the KplE1 prophage, site-specific recombination is mediated by the IntS integrase and the TorI recombination directionality factor (RDF). We previously described a sub-family of temperate phages that is characterized by an unusual organization of the recombination module. Consequently, the attL recombination region overlaps with the integrase promoter, and the integrase and RDF genes do not share a common activated promoter upon lytic induction as in the lambda prophage. In this study, we show that the intS gene is tightly regulated by its own product as well as by the TorI RDF protein. In silico analysis revealed that overlap of the attL region with the integrase promoter is widely encountered in prophages present in prokaryotic genomes, suggesting a general occurrence of negatively autoregulated integrase genes. The prediction that these integrase genes are negatively autoregulated was biologically assessed by studying the regulation of several integrase genes from two different Escherichia coli strains. Our results suggest that the majority of tRNA-associated integrase genes in prokaryotic genomes could be autoregulated and that this might be correlated with the recombination efficiency as in KplE1. The consequences of this unprecedented regulation for excessive recombination are discussed.http://europepmc.org/articles/PMC2951348?pdf=render
spellingShingle Gaël Panis
Yohann Duverger
Elise Courvoisier-Dezord
Stéphanie Champ
Emmanuel Talla
Mireille Ansaldi
Tight regulation of the intS gene of the KplE1 prophage: a new paradigm for integrase gene regulation.
PLoS Genetics
title Tight regulation of the intS gene of the KplE1 prophage: a new paradigm for integrase gene regulation.
title_full Tight regulation of the intS gene of the KplE1 prophage: a new paradigm for integrase gene regulation.
title_fullStr Tight regulation of the intS gene of the KplE1 prophage: a new paradigm for integrase gene regulation.
title_full_unstemmed Tight regulation of the intS gene of the KplE1 prophage: a new paradigm for integrase gene regulation.
title_short Tight regulation of the intS gene of the KplE1 prophage: a new paradigm for integrase gene regulation.
title_sort tight regulation of the ints gene of the kple1 prophage a new paradigm for integrase gene regulation
url http://europepmc.org/articles/PMC2951348?pdf=render
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