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...
| Main Authors: | , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2012-01-01
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| Series: | PLoS Pathogens |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23209414/?tool=EBI |
| _version_ | 1818388176889184256 |
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| 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 |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-12-14T04:21:41Z |
| format | Article |
| id | doaj.art-9a84fb1f49484d7198d453a5cb35b5c9 |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-12-14T04:21:41Z |
| publishDate | 2012-01-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-9a84fb1f49484d7198d453a5cb35b5c92022-12-21T23:17:20ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742012-01-01811e100304310.1371/journal.ppat.1003043A trade-off between the fitness cost of functional integrases and long-term stability of integrons.Irina StarikovaKlaus HarmsPål HaugenTracy T M LundeRaul PrimicerioØrjan SamuelsenKaare M NielsenPål J JohnsenHorizontal 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.https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23209414/?tool=EBI |
| spellingShingle | 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. PLoS Pathogens |
| title | 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_short | 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 |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/pmid/23209414/?tool=EBI |
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