Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors.

Many species of bacteria harbor multiple prophages in their genomes. Prophages often carry genes that confer a selective advantage to the bacterium, typically during host colonization. Prophages can convert to infectious viruses through a process known as induction, which is relevant to the spread o...

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Main Authors: Sébastien Lemire, Nara Figueroa-Bossi, Lionello Bossi
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2011-06-01
Series:PLoS Genetics
Online Access:http://europepmc.org/articles/PMC3121763?pdf=render
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spelling doaj-15c011e6b77f4efe98febc73e2a0858c2020-11-24T22:19:26ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042011-06-0176e100214910.1371/journal.pgen.1002149Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors.Sébastien LemireNara Figueroa-BossiLionello BossiMany species of bacteria harbor multiple prophages in their genomes. Prophages often carry genes that confer a selective advantage to the bacterium, typically during host colonization. Prophages can convert to infectious viruses through a process known as induction, which is relevant to the spread of bacterial virulence genes. The paradigm of prophage induction, as set by the phage Lambda model, sees the process initiated by the RecA-stimulated self-proteolysis of the phage repressor. Here we show that a large family of lambdoid prophages found in Salmonella genomes employs an alternative induction strategy. The repressors of these phages are not cleaved upon induction; rather, they are inactivated by the binding of small antirepressor proteins. Formation of the complex causes the repressor to dissociate from DNA. The antirepressor genes lie outside the immunity region and are under direct control of the LexA repressor, thus plugging prophage induction directly into the SOS response. GfoA and GfhA, the antirepressors of Salmonella prophages Gifsy-1 and Gifsy-3, each target both of these phages' repressors, GfoR and GfhR, even though the latter proteins recognize different operator sites and the two phages are heteroimmune. In contrast, the Gifsy-2 phage repressor, GtgR, is insensitive to GfoA and GfhA, but is inactivated by an antirepressor from the unrelated Fels-1 prophage (FsoA). This response is all the more surprising as FsoA is under the control of the Fels-1 repressor, not LexA, and plays no apparent role in Fels-1 induction, which occurs via a Lambda CI-like repressor cleavage mechanism. The ability of antirepressors to recognize non-cognate repressors allows coordination of induction of multiple prophages in polylysogenic strains. Identification of non-cleavable gfoR/gtgR homologues in a large variety of bacterial genomes (including most Escherichia coli genomes in the DNA database) suggests that antirepression-mediated induction is far more common than previously recognized.http://europepmc.org/articles/PMC3121763?pdf=render
collection DOAJ
language English
format Article
sources DOAJ
author Sébastien Lemire
Nara Figueroa-Bossi
Lionello Bossi
spellingShingle Sébastien Lemire
Nara Figueroa-Bossi
Lionello Bossi
Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors.
PLoS Genetics
author_facet Sébastien Lemire
Nara Figueroa-Bossi
Lionello Bossi
author_sort Sébastien Lemire
title Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors.
title_short Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors.
title_full Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors.
title_fullStr Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors.
title_full_unstemmed Bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors.
title_sort bacteriophage crosstalk: coordination of prophage induction by trans-acting antirepressors.
publisher Public Library of Science (PLoS)
series PLoS Genetics
issn 1553-7390
1553-7404
publishDate 2011-06-01
description Many species of bacteria harbor multiple prophages in their genomes. Prophages often carry genes that confer a selective advantage to the bacterium, typically during host colonization. Prophages can convert to infectious viruses through a process known as induction, which is relevant to the spread of bacterial virulence genes. The paradigm of prophage induction, as set by the phage Lambda model, sees the process initiated by the RecA-stimulated self-proteolysis of the phage repressor. Here we show that a large family of lambdoid prophages found in Salmonella genomes employs an alternative induction strategy. The repressors of these phages are not cleaved upon induction; rather, they are inactivated by the binding of small antirepressor proteins. Formation of the complex causes the repressor to dissociate from DNA. The antirepressor genes lie outside the immunity region and are under direct control of the LexA repressor, thus plugging prophage induction directly into the SOS response. GfoA and GfhA, the antirepressors of Salmonella prophages Gifsy-1 and Gifsy-3, each target both of these phages' repressors, GfoR and GfhR, even though the latter proteins recognize different operator sites and the two phages are heteroimmune. In contrast, the Gifsy-2 phage repressor, GtgR, is insensitive to GfoA and GfhA, but is inactivated by an antirepressor from the unrelated Fels-1 prophage (FsoA). This response is all the more surprising as FsoA is under the control of the Fels-1 repressor, not LexA, and plays no apparent role in Fels-1 induction, which occurs via a Lambda CI-like repressor cleavage mechanism. The ability of antirepressors to recognize non-cognate repressors allows coordination of induction of multiple prophages in polylysogenic strains. Identification of non-cleavable gfoR/gtgR homologues in a large variety of bacterial genomes (including most Escherichia coli genomes in the DNA database) suggests that antirepression-mediated induction is far more common than previously recognized.
url http://europepmc.org/articles/PMC3121763?pdf=render
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