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Translational demand is not a major source of plasmid-associated fitness costs

Plasmids are key drivers of bacterial evolution because they are crucial agents for the horizontal transfer of adaptive traits, such as antibiotic resistance. Most plasmids entail a metabolic burden that reduces the fitness of their host if there is no selection for plasmid-encoded genes. It has bee...

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Autores principales: Rodríguez-Beltrán, Jerónimo, León-Sampedro, Ricardo, Ramiro-Martínez, Paula, de la Vega, Carmen, Baquero, Fernando, Levin, Bruce R., San Millán, Álvaro
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8628068/
https://www.ncbi.nlm.nih.gov/pubmed/34839712
http://dx.doi.org/10.1098/rstb.2020.0463
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author Rodríguez-Beltrán, Jerónimo
León-Sampedro, Ricardo
Ramiro-Martínez, Paula
de la Vega, Carmen
Baquero, Fernando
Levin, Bruce R.
San Millán, Álvaro
author_facet Rodríguez-Beltrán, Jerónimo
León-Sampedro, Ricardo
Ramiro-Martínez, Paula
de la Vega, Carmen
Baquero, Fernando
Levin, Bruce R.
San Millán, Álvaro
author_sort Rodríguez-Beltrán, Jerónimo
collection PubMed
description Plasmids are key drivers of bacterial evolution because they are crucial agents for the horizontal transfer of adaptive traits, such as antibiotic resistance. Most plasmids entail a metabolic burden that reduces the fitness of their host if there is no selection for plasmid-encoded genes. It has been hypothesized that the translational demand imposed by plasmid-encoded genes is a major mechanism driving the fitness cost of plasmids. Plasmid-encoded genes typically present a different codon usage from host chromosomal genes. As a consequence, the translation of plasmid-encoded genes might sequestrate ribosomes on plasmid transcripts, overwhelming the translation machinery of the cell. However, the pervasiveness and origins of the translation-derived costs of plasmids are yet to be assessed. Here, we systematically altered translation efficiency in the host cell to disentangle the fitness effects produced by six natural antibiotic resistance plasmids. We show that limiting translation efficiency either by reducing the number of available ribosomes or their processivity does not increase plasmid costs. Overall, our results suggest that ribosomal paucity is not a major contributor to plasmid fitness costs. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’.
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spelling pubmed-86280682021-12-23 Translational demand is not a major source of plasmid-associated fitness costs Rodríguez-Beltrán, Jerónimo León-Sampedro, Ricardo Ramiro-Martínez, Paula de la Vega, Carmen Baquero, Fernando Levin, Bruce R. San Millán, Álvaro Philos Trans R Soc Lond B Biol Sci Articles Plasmids are key drivers of bacterial evolution because they are crucial agents for the horizontal transfer of adaptive traits, such as antibiotic resistance. Most plasmids entail a metabolic burden that reduces the fitness of their host if there is no selection for plasmid-encoded genes. It has been hypothesized that the translational demand imposed by plasmid-encoded genes is a major mechanism driving the fitness cost of plasmids. Plasmid-encoded genes typically present a different codon usage from host chromosomal genes. As a consequence, the translation of plasmid-encoded genes might sequestrate ribosomes on plasmid transcripts, overwhelming the translation machinery of the cell. However, the pervasiveness and origins of the translation-derived costs of plasmids are yet to be assessed. Here, we systematically altered translation efficiency in the host cell to disentangle the fitness effects produced by six natural antibiotic resistance plasmids. We show that limiting translation efficiency either by reducing the number of available ribosomes or their processivity does not increase plasmid costs. Overall, our results suggest that ribosomal paucity is not a major contributor to plasmid fitness costs. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’. The Royal Society 2022-01-17 2021-11-29 /pmc/articles/PMC8628068/ /pubmed/34839712 http://dx.doi.org/10.1098/rstb.2020.0463 Text en © 2021 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited.
spellingShingle Articles
Rodríguez-Beltrán, Jerónimo
León-Sampedro, Ricardo
Ramiro-Martínez, Paula
de la Vega, Carmen
Baquero, Fernando
Levin, Bruce R.
San Millán, Álvaro
Translational demand is not a major source of plasmid-associated fitness costs
title Translational demand is not a major source of plasmid-associated fitness costs
title_full Translational demand is not a major source of plasmid-associated fitness costs
title_fullStr Translational demand is not a major source of plasmid-associated fitness costs
title_full_unstemmed Translational demand is not a major source of plasmid-associated fitness costs
title_short Translational demand is not a major source of plasmid-associated fitness costs
title_sort translational demand is not a major source of plasmid-associated fitness costs
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8628068/
https://www.ncbi.nlm.nih.gov/pubmed/34839712
http://dx.doi.org/10.1098/rstb.2020.0463
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