Toxin-antitoxin gene pairs found in Tn3 family transposons appear to be an integral part of the transposition module
Autor(a) principal: | |
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Data de Publicação: | 2020 |
Outros Autores: | , , , , , |
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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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:29462024-08-05T17:14:43.213908Repositório 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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1808128778608574464 |