A trade-off between the fitness cost of functional integrases and long-term stability of integrons.

Horizontal gene transfer (HGT) plays a major role in bacterial microevolution as evident from the rapid emergence and spread of antimicrobial drug resistance. Few studies have however addressed the population dynamics of newly imported genetic elements after HGT. Here, we show that newly acquired cl...

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Autores principales: Irina Starikova, Klaus Harms, Pål Haugen, Tracy T M Lunde, Raul Primicerio, Ørjan Samuelsen, Kaare M Nielsen, Pål J Johnsen
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Publicado: Public Library of Science (PLoS) 2012
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Acceso en línea:https://doaj.org/article/9a84fb1f49484d7198d453a5cb35b5c9
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spelling oai:doaj.org-article:9a84fb1f49484d7198d453a5cb35b5c92021-11-18T06:06:19ZA trade-off between the fitness cost of functional integrases and long-term stability of integrons.1553-73661553-737410.1371/journal.ppat.1003043https://doaj.org/article/9a84fb1f49484d7198d453a5cb35b5c92012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23209414/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374Horizontal gene transfer (HGT) plays a major role in bacterial microevolution as evident from the rapid emergence and spread of antimicrobial drug resistance. Few studies have however addressed the population dynamics of newly imported genetic elements after HGT. Here, we show that newly acquired class-1 integrons from Salmonella enterica serovar Typhimurium and Acinetobacter baumannii, free of associated transposable elements, strongly reduce host fitness in Acinetobacter baylyi. Insertional inactivation of the integron intI1 restored fitness, demonstrating that the observed fitness costs were due to the presence of an active integrase. The biological cost of harboring class-1 integrons was rapidly reduced during serial transfers due to intI1 frameshift mutations leading to inactivated integrases. We use a mathematical model to explore the conditions where integrons with functional integrases are maintained and conclude that environmental fluctuations and episodic selection is necessary for the maintenance of functional integrases. Taken together, the presented data suggest a trade-off between the ability to capture gene cassettes and long-term stability of integrons and provide an explanation for the frequent observation of inactive integron-integrases in bacterial populations.Irina StarikovaKlaus HarmsPål HaugenTracy T M LundeRaul PrimicerioØrjan SamuelsenKaare M NielsenPål J JohnsenPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 8, Iss 11, p e1003043 (2012)
institution DOAJ
collection DOAJ
language EN
topic Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
spellingShingle Immunologic diseases. Allergy
RC581-607
Biology (General)
QH301-705.5
Irina Starikova
Klaus Harms
Pål Haugen
Tracy T M Lunde
Raul Primicerio
Ørjan Samuelsen
Kaare M Nielsen
Pål J Johnsen
A trade-off between the fitness cost of functional integrases and long-term stability of integrons.
description Horizontal gene transfer (HGT) plays a major role in bacterial microevolution as evident from the rapid emergence and spread of antimicrobial drug resistance. Few studies have however addressed the population dynamics of newly imported genetic elements after HGT. Here, we show that newly acquired class-1 integrons from Salmonella enterica serovar Typhimurium and Acinetobacter baumannii, free of associated transposable elements, strongly reduce host fitness in Acinetobacter baylyi. Insertional inactivation of the integron intI1 restored fitness, demonstrating that the observed fitness costs were due to the presence of an active integrase. The biological cost of harboring class-1 integrons was rapidly reduced during serial transfers due to intI1 frameshift mutations leading to inactivated integrases. We use a mathematical model to explore the conditions where integrons with functional integrases are maintained and conclude that environmental fluctuations and episodic selection is necessary for the maintenance of functional integrases. Taken together, the presented data suggest a trade-off between the ability to capture gene cassettes and long-term stability of integrons and provide an explanation for the frequent observation of inactive integron-integrases in bacterial populations.
format article
author Irina Starikova
Klaus Harms
Pål Haugen
Tracy T M Lunde
Raul Primicerio
Ørjan Samuelsen
Kaare M Nielsen
Pål J Johnsen
author_facet Irina Starikova
Klaus Harms
Pål Haugen
Tracy T M Lunde
Raul Primicerio
Ørjan Samuelsen
Kaare M Nielsen
Pål J Johnsen
author_sort Irina Starikova
title A trade-off between the fitness cost of functional integrases and long-term stability of integrons.
title_short A trade-off between the fitness cost of functional integrases and long-term stability of integrons.
title_full A trade-off between the fitness cost of functional integrases and long-term stability of integrons.
title_fullStr A trade-off between the fitness cost of functional integrases and long-term stability of integrons.
title_full_unstemmed A trade-off between the fitness cost of functional integrases and long-term stability of integrons.
title_sort trade-off between the fitness cost of functional integrases and long-term stability of integrons.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/9a84fb1f49484d7198d453a5cb35b5c9
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