Toxin-Antitoxin Gene Pairs Found in Tn<italic toggle="yes">3</italic> Family Transposons Appear To Be an Integral Part of the Transposition Module

ABSTRACT Much of the diversity of prokaryotic genomes is contributed by the tightly controlled recombination activity of transposons (Tns). The Tn3 family is arguably one of the most widespread transposon families. Members carry a large range of passenger genes incorporated into their structures. Fa...

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Autores principales:	Gipsi Lima-Mendez, Danillo Oliveira Alvarenga, Karen Ross, Bernard Hallet, Laurence Van Melderen, Alessandro M. Varani, Michael Chandler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	antitoxin Tn3 family toxin transposition Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/c0e047765c084cb486222d54c62a97f6
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spelling	oai:doaj.org-article:c0e047765c084cb486222d54c62a97f62021-11-15T15:57:02ZToxin-Antitoxin Gene Pairs Found in Tn<italic toggle="yes">3</italic> Family Transposons Appear To Be an Integral Part of the Transposition Module10.1128/mBio.00452-202150-7511https://doaj.org/article/c0e047765c084cb486222d54c62a97f62020-04-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00452-20https://doaj.org/toc/2150-7511ABSTRACT Much of the diversity of prokaryotic genomes is contributed by the tightly controlled recombination activity of transposons (Tns). The Tn3 family is arguably one of the most widespread transposon families. Members carry a large range of passenger genes incorporated into their structures. Family members undergo replicative transposition using a DDE transposase to generate a cointegrate structure which is then resolved by site-specific recombination between specific DNA sequences (res) on each of the two Tn copies in the cointegrate. These sites also carry promoters controlling expression of the recombinase and transposase. We report here that a number of Tn3 members encode a type II toxin-antitoxin (TA) system, typically composed of a stable toxin and a labile antitoxin that binds the toxin and inhibits its lethal activity. This system serves to improve plasmid maintenance in a bacterial population and, until recently, was believed to be associated with bacterial persistence. At least six different TA gene pairs are associated with various Tn3 members. Our data suggest that several independent acquisition events have occurred. In contrast to most Tn3 family passenger genes, which are generally located away from the transposition module, the TA gene pairs abut the res site upstream of the resolvase genes. Although their role when part of Tn3 family transposons is unclear, this finding suggests a potential role for the embedded TA in stabilizing the associated transposon with the possibility that TA expression is coupled to expression of transposase and resolvase during the transposition process itself. IMPORTANCE Transposable elements (TEs) are important in genetic diversification due to their recombination properties and their ability to promote horizontal gene transfer. Over the last decades, much effort has been made to understand TE transposition mechanisms and their impact on prokaryotic genomes. For example, the Tn3 family is ubiquitous in bacteria, molding their host genomes by the paste-and-copy mechanism. In addition to the transposition module, Tn3 members often carry additional passenger genes (e.g., conferring antibiotic or heavy metal resistance and virulence), and three were previously known to carry a toxin-antitoxin (TA) system often associated with plasmid maintenance; however, the role of TA systems within the Tn3 family is unknown. The genetic context of TA systems in Tn3 members suggests that they may play a regulatory role in ensuring stable invasion of these Tns during transposition.Gipsi Lima-MendezDanillo Oliveira AlvarengaKaren RossBernard HalletLaurence Van MelderenAlessandro M. VaraniMichael ChandlerAmerican Society for MicrobiologyarticleantitoxinTn3 familytoxintranspositionMicrobiologyQR1-502ENmBio, Vol 11, Iss 2 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	antitoxin Tn3 family toxin transposition Microbiology QR1-502
spellingShingle	antitoxin Tn3 family toxin transposition Microbiology QR1-502 Gipsi Lima-Mendez Danillo Oliveira Alvarenga Karen Ross Bernard Hallet Laurence Van Melderen Alessandro M. Varani Michael Chandler Toxin-Antitoxin Gene Pairs Found in Tn<italic toggle="yes">3</italic> Family Transposons Appear To Be an Integral Part of the Transposition Module
description	ABSTRACT Much of the diversity of prokaryotic genomes is contributed by the tightly controlled recombination activity of transposons (Tns). The Tn3 family is arguably one of the most widespread transposon families. Members carry a large range of passenger genes incorporated into their structures. Family members undergo replicative transposition using a DDE transposase to generate a cointegrate structure which is then resolved by site-specific recombination between specific DNA sequences (res) on each of the two Tn copies in the cointegrate. These sites also carry promoters controlling expression of the recombinase and transposase. We report here that a number of Tn3 members encode a type II toxin-antitoxin (TA) system, typically composed of a stable toxin and a labile antitoxin that binds the toxin and inhibits its lethal activity. This system serves to improve plasmid maintenance in a bacterial population and, until recently, was believed to be associated with bacterial persistence. At least six different TA gene pairs are associated with various Tn3 members. Our data suggest that several independent acquisition events have occurred. In contrast to most Tn3 family passenger genes, which are generally located away from the transposition module, the TA gene pairs abut the res site upstream of the resolvase genes. Although their role when part of Tn3 family transposons is unclear, this finding suggests a potential role for the embedded TA in stabilizing the associated transposon with the possibility that TA expression is coupled to expression of transposase and resolvase during the transposition process itself. IMPORTANCE Transposable elements (TEs) are important in genetic diversification due to their recombination properties and their ability to promote horizontal gene transfer. Over the last decades, much effort has been made to understand TE transposition mechanisms and their impact on prokaryotic genomes. For example, the Tn3 family is ubiquitous in bacteria, molding their host genomes by the paste-and-copy mechanism. In addition to the transposition module, Tn3 members often carry additional passenger genes (e.g., conferring antibiotic or heavy metal resistance and virulence), and three were previously known to carry a toxin-antitoxin (TA) system often associated with plasmid maintenance; however, the role of TA systems within the Tn3 family is unknown. The genetic context of TA systems in Tn3 members suggests that they may play a regulatory role in ensuring stable invasion of these Tns during transposition.
format	article
author	Gipsi Lima-Mendez Danillo Oliveira Alvarenga Karen Ross Bernard Hallet Laurence Van Melderen Alessandro M. Varani Michael Chandler
author_facet	Gipsi Lima-Mendez Danillo Oliveira Alvarenga Karen Ross Bernard Hallet Laurence Van Melderen Alessandro M. Varani Michael Chandler
author_sort	Gipsi Lima-Mendez
title	Toxin-Antitoxin Gene Pairs Found in Tn<italic toggle="yes">3</italic> Family Transposons Appear To Be an Integral Part of the Transposition Module
title_short	Toxin-Antitoxin Gene Pairs Found in Tn<italic toggle="yes">3</italic> Family Transposons Appear To Be an Integral Part of the Transposition Module
title_full	Toxin-Antitoxin Gene Pairs Found in Tn<italic toggle="yes">3</italic> Family Transposons Appear To Be an Integral Part of the Transposition Module
title_fullStr	Toxin-Antitoxin Gene Pairs Found in Tn<italic toggle="yes">3</italic> Family Transposons Appear To Be an Integral Part of the Transposition Module
title_full_unstemmed	Toxin-Antitoxin Gene Pairs Found in Tn<italic toggle="yes">3</italic> Family Transposons Appear To Be an Integral Part of the Transposition Module
title_sort	toxin-antitoxin gene pairs found in tn<italic toggle="yes">3</italic> family transposons appear to be an integral part of the transposition module
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/c0e047765c084cb486222d54c62a97f6
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Toxin-Antitoxin Gene Pairs Found in Tn<italic toggle="yes">3</italic> Family Transposons Appear To Be an Integral Part of the Transposition Module

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