Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module

Detalhes bibliográficos
Autor(a) principal: Lima-Mendez, Gipsi
Data de Publicação: 2020
Outros Autores: Alvarenga, Danillo Oliveira [UNESP], Ross, Karen, Hallet, Bernard, Van Melderen, Laurence, Varani, Alessandro M. [UNESP], Chandler, Michael
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNESP
Texto Completo: http://dx.doi.org/10.1128/mBio.00452-20
http://hdl.handle.net/11449/221453
Resumo: Much of the diversity of prokaryotic genomes is contributed by the tightly controlled recombination activity of transposons (Tns). The Tn3 family is argu-ably one of the most widespread transposon families. Members carry a large range of passenger genes incorporated into their structures. Family members undergo rep-licative 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 oc-curred. 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 un-clear, 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 plas-mid 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.
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spelling Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition moduleAntitoxinTn3 familyToxinTranspositionMuch of the diversity of prokaryotic genomes is contributed by the tightly controlled recombination activity of transposons (Tns). The Tn3 family is argu-ably one of the most widespread transposon families. Members carry a large range of passenger genes incorporated into their structures. Family members undergo rep-licative 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 oc-curred. 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 un-clear, 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 plas-mid 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.Cellular and Molecular Microbiology (CM2) Faculté des Sciences Université Libre de Bruxelles (ULB)School of Agricultural and Veterinary Sciences Universidade Estadual PaulistaProtein Information Resource Department of Biochemistry Molecular and Cellular Biology Georgetown University Medical CenterLouvain Institute of Biomolecular Science and Technology Université Catholique de Louvain (UCLouvain)Department of Biochemistry Molecular and Cellular Biology Georgetown University Medical CenterSchool of Agricultural and Veterinary Sciences Universidade Estadual PaulistaUniversité Libre de Bruxelles (ULB)Universidade Estadual Paulista (UNESP)Georgetown University Medical CenterUniversité Catholique de Louvain (UCLouvain)Lima-Mendez, GipsiAlvarenga, Danillo Oliveira [UNESP]Ross, KarenHallet, BernardVan Melderen, LaurenceVarani, Alessandro M. [UNESP]Chandler, Michael2022-04-28T19:28:33Z2022-04-28T19:28:33Z2020-03-01info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1128/mBio.00452-20mBio, v. 11, n. 2, 2020.2150-75112161-2129http://hdl.handle.net/11449/22145310.1128/mBio.00452-202-s2.0-85082731807Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengmBioinfo:eu-repo/semantics/openAccess2022-04-28T19:28:33Zoai:repositorio.unesp.br:11449/221453Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462022-04-28T19:28:33Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false
dc.title.none.fl_str_mv Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module
title Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module
spellingShingle Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module
Lima-Mendez, Gipsi
Antitoxin
Tn3 family
Toxin
Transposition
title_short Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module
title_full Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module
title_fullStr Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module
title_full_unstemmed Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module
title_sort Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module
author Lima-Mendez, Gipsi
author_facet Lima-Mendez, Gipsi
Alvarenga, Danillo Oliveira [UNESP]
Ross, Karen
Hallet, Bernard
Van Melderen, Laurence
Varani, Alessandro M. [UNESP]
Chandler, Michael
author_role author
author2 Alvarenga, Danillo Oliveira [UNESP]
Ross, Karen
Hallet, Bernard
Van Melderen, Laurence
Varani, Alessandro M. [UNESP]
Chandler, Michael
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Université Libre de Bruxelles (ULB)
Universidade Estadual Paulista (UNESP)
Georgetown University Medical Center
Université Catholique de Louvain (UCLouvain)
dc.contributor.author.fl_str_mv Lima-Mendez, Gipsi
Alvarenga, Danillo Oliveira [UNESP]
Ross, Karen
Hallet, Bernard
Van Melderen, Laurence
Varani, Alessandro M. [UNESP]
Chandler, Michael
dc.subject.por.fl_str_mv Antitoxin
Tn3 family
Toxin
Transposition
topic Antitoxin
Tn3 family
Toxin
Transposition
description Much of the diversity of prokaryotic genomes is contributed by the tightly controlled recombination activity of transposons (Tns). The Tn3 family is argu-ably one of the most widespread transposon families. Members carry a large range of passenger genes incorporated into their structures. Family members undergo rep-licative 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 oc-curred. 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 un-clear, 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 plas-mid 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.
publishDate 2020
dc.date.none.fl_str_mv 2020-03-01
2022-04-28T19:28:33Z
2022-04-28T19:28:33Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1128/mBio.00452-20
mBio, v. 11, n. 2, 2020.
2150-7511
2161-2129
http://hdl.handle.net/11449/221453
10.1128/mBio.00452-20
2-s2.0-85082731807
url http://dx.doi.org/10.1128/mBio.00452-20
http://hdl.handle.net/11449/221453
identifier_str_mv mBio, v. 11, n. 2, 2020.
2150-7511
2161-2129
10.1128/mBio.00452-20
2-s2.0-85082731807
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv mBio
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.source.none.fl_str_mv Scopus
reponame:Repositório Institucional da UNESP
instname:Universidade Estadual Paulista (UNESP)
instacron:UNESP
instname_str Universidade Estadual Paulista (UNESP)
instacron_str UNESP
institution UNESP
reponame_str Repositório Institucional da UNESP
collection Repositório Institucional da UNESP
repository.name.fl_str_mv Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)
repository.mail.fl_str_mv
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