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Evolution of satellite plasmids can prolong the maintenance of newly acquired accessory genes in bacteria

Transmissible plasmids spread genes encoding antibiotic resistance and other traits to new bacterial species. Here we report that laboratory populations of Escherichia coli with a newly acquired IncQ plasmid often evolve ‘satellite plasmids’ with deletions of accessory genes and genes required for p...

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Autores principales: Zhang, Xue, Deatherage, Daniel E., Zheng, Hao, Georgoulis, Stratton J., Barrick, Jeffrey E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6925257/
https://www.ncbi.nlm.nih.gov/pubmed/31863068
http://dx.doi.org/10.1038/s41467-019-13709-x
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author Zhang, Xue
Deatherage, Daniel E.
Zheng, Hao
Georgoulis, Stratton J.
Barrick, Jeffrey E.
author_facet Zhang, Xue
Deatherage, Daniel E.
Zheng, Hao
Georgoulis, Stratton J.
Barrick, Jeffrey E.
author_sort Zhang, Xue
collection PubMed
description Transmissible plasmids spread genes encoding antibiotic resistance and other traits to new bacterial species. Here we report that laboratory populations of Escherichia coli with a newly acquired IncQ plasmid often evolve ‘satellite plasmids’ with deletions of accessory genes and genes required for plasmid replication. Satellite plasmids are molecular parasites: their presence reduces the copy number of the full-length plasmid on which they rely for their continued replication. Cells with satellite plasmids gain an immediate fitness advantage from reducing burdensome expression of accessory genes. Yet, they maintain copies of these genes and the complete plasmid, which potentially enables them to benefit from and transmit the traits they encode in the future. Evolution of satellite plasmids is transient. Cells that entirely lose accessory gene function or plasmid mobility dominate in the long run. Satellite plasmids also evolve in Snodgrassella alvi colonizing the honey bee gut, suggesting that this mechanism may broadly contribute to the importance of IncQ plasmids as agents of bacterial gene transfer in nature.
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spelling pubmed-69252572019-12-22 Evolution of satellite plasmids can prolong the maintenance of newly acquired accessory genes in bacteria Zhang, Xue Deatherage, Daniel E. Zheng, Hao Georgoulis, Stratton J. Barrick, Jeffrey E. Nat Commun Article Transmissible plasmids spread genes encoding antibiotic resistance and other traits to new bacterial species. Here we report that laboratory populations of Escherichia coli with a newly acquired IncQ plasmid often evolve ‘satellite plasmids’ with deletions of accessory genes and genes required for plasmid replication. Satellite plasmids are molecular parasites: their presence reduces the copy number of the full-length plasmid on which they rely for their continued replication. Cells with satellite plasmids gain an immediate fitness advantage from reducing burdensome expression of accessory genes. Yet, they maintain copies of these genes and the complete plasmid, which potentially enables them to benefit from and transmit the traits they encode in the future. Evolution of satellite plasmids is transient. Cells that entirely lose accessory gene function or plasmid mobility dominate in the long run. Satellite plasmids also evolve in Snodgrassella alvi colonizing the honey bee gut, suggesting that this mechanism may broadly contribute to the importance of IncQ plasmids as agents of bacterial gene transfer in nature. Nature Publishing Group UK 2019-12-20 /pmc/articles/PMC6925257/ /pubmed/31863068 http://dx.doi.org/10.1038/s41467-019-13709-x Text en © The Author(s) 2019 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.
spellingShingle Article
Zhang, Xue
Deatherage, Daniel E.
Zheng, Hao
Georgoulis, Stratton J.
Barrick, Jeffrey E.
Evolution of satellite plasmids can prolong the maintenance of newly acquired accessory genes in bacteria
title Evolution of satellite plasmids can prolong the maintenance of newly acquired accessory genes in bacteria
title_full Evolution of satellite plasmids can prolong the maintenance of newly acquired accessory genes in bacteria
title_fullStr Evolution of satellite plasmids can prolong the maintenance of newly acquired accessory genes in bacteria
title_full_unstemmed Evolution of satellite plasmids can prolong the maintenance of newly acquired accessory genes in bacteria
title_short Evolution of satellite plasmids can prolong the maintenance of newly acquired accessory genes in bacteria
title_sort evolution of satellite plasmids can prolong the maintenance of newly acquired accessory genes in bacteria
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6925257/
https://www.ncbi.nlm.nih.gov/pubmed/31863068
http://dx.doi.org/10.1038/s41467-019-13709-x
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