Cargando…

Compensatory mutations improve general permissiveness to antibiotic resistance plasmids

Horizontal gene transfer mediated by broad-host-range plasmids is an important mechanism of antibiotic resistance spread. While not all bacteria maintain plasmids equally well, plasmid persistence can improve over time, yet no general evolutionary mechanisms have emerged. Our goal was to identify th...

Descripción completa

Detalles Bibliográficos
Autores principales: Loftie-Eaton, Wesley, Bashford, Kelsie, Quinn, Hannah, Dong, Kieran, Millstein, Jack, Hunter, Samuel, Thomason, Maureen K., Merrikh, Houra, Ponciano, Jose M., Top, Eva M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: 2017
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5649373/
https://www.ncbi.nlm.nih.gov/pubmed/29046540
http://dx.doi.org/10.1038/s41559-017-0243-2
_version_ 1783272535162355712
author Loftie-Eaton, Wesley
Bashford, Kelsie
Quinn, Hannah
Dong, Kieran
Millstein, Jack
Hunter, Samuel
Thomason, Maureen K.
Merrikh, Houra
Ponciano, Jose M.
Top, Eva M.
author_facet Loftie-Eaton, Wesley
Bashford, Kelsie
Quinn, Hannah
Dong, Kieran
Millstein, Jack
Hunter, Samuel
Thomason, Maureen K.
Merrikh, Houra
Ponciano, Jose M.
Top, Eva M.
author_sort Loftie-Eaton, Wesley
collection PubMed
description Horizontal gene transfer mediated by broad-host-range plasmids is an important mechanism of antibiotic resistance spread. While not all bacteria maintain plasmids equally well, plasmid persistence can improve over time, yet no general evolutionary mechanisms have emerged. Our goal was to identify these mechanisms, and to assess if adaptation to one plasmid affects the permissiveness to others. We experimentally evolved Pseudomonas sp. H2 containing multi-drug resistance plasmid RP4, determined plasmid persistence and cost using a joint experimental-modeling approach, resequenced evolved clones, and reconstructed key mutations. Plasmid persistence improved in fewer than 600 generations because the fitness cost turned into a benefit. Improved retention of naive plasmids indicated that the host evolved towards increased plasmid permissiveness. Key chromosomal mutations affected two accessory helicases and the RNA polymerase β-subunit. Our and other findings suggest that poor plasmid persistence can be caused by a high cost involving helicase-plasmid interactions that can be rapidly ameliorated.
format Online
Article
Text
id pubmed-5649373
institution National Center for Biotechnology Information
language English
publishDate 2017
record_format MEDLINE/PubMed
spelling pubmed-56493732018-02-07 Compensatory mutations improve general permissiveness to antibiotic resistance plasmids Loftie-Eaton, Wesley Bashford, Kelsie Quinn, Hannah Dong, Kieran Millstein, Jack Hunter, Samuel Thomason, Maureen K. Merrikh, Houra Ponciano, Jose M. Top, Eva M. Nat Ecol Evol Article Horizontal gene transfer mediated by broad-host-range plasmids is an important mechanism of antibiotic resistance spread. While not all bacteria maintain plasmids equally well, plasmid persistence can improve over time, yet no general evolutionary mechanisms have emerged. Our goal was to identify these mechanisms, and to assess if adaptation to one plasmid affects the permissiveness to others. We experimentally evolved Pseudomonas sp. H2 containing multi-drug resistance plasmid RP4, determined plasmid persistence and cost using a joint experimental-modeling approach, resequenced evolved clones, and reconstructed key mutations. Plasmid persistence improved in fewer than 600 generations because the fitness cost turned into a benefit. Improved retention of naive plasmids indicated that the host evolved towards increased plasmid permissiveness. Key chromosomal mutations affected two accessory helicases and the RNA polymerase β-subunit. Our and other findings suggest that poor plasmid persistence can be caused by a high cost involving helicase-plasmid interactions that can be rapidly ameliorated. 2017-08-07 2017-09 /pmc/articles/PMC5649373/ /pubmed/29046540 http://dx.doi.org/10.1038/s41559-017-0243-2 Text en Users may view, print, copy, and download text and data-mine the content in such documents, for the purposes of academic research, subject always to the full Conditions of use: http://www.nature.com/authors/editorial_policies/license.html#terms
spellingShingle Article
Loftie-Eaton, Wesley
Bashford, Kelsie
Quinn, Hannah
Dong, Kieran
Millstein, Jack
Hunter, Samuel
Thomason, Maureen K.
Merrikh, Houra
Ponciano, Jose M.
Top, Eva M.
Compensatory mutations improve general permissiveness to antibiotic resistance plasmids
title Compensatory mutations improve general permissiveness to antibiotic resistance plasmids
title_full Compensatory mutations improve general permissiveness to antibiotic resistance plasmids
title_fullStr Compensatory mutations improve general permissiveness to antibiotic resistance plasmids
title_full_unstemmed Compensatory mutations improve general permissiveness to antibiotic resistance plasmids
title_short Compensatory mutations improve general permissiveness to antibiotic resistance plasmids
title_sort compensatory mutations improve general permissiveness to antibiotic resistance plasmids
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5649373/
https://www.ncbi.nlm.nih.gov/pubmed/29046540
http://dx.doi.org/10.1038/s41559-017-0243-2
work_keys_str_mv AT loftieeatonwesley compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids
AT bashfordkelsie compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids
AT quinnhannah compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids
AT dongkieran compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids
AT millsteinjack compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids
AT huntersamuel compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids
AT thomasonmaureenk compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids
AT merrikhhoura compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids
AT poncianojosem compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids
AT topevam compensatorymutationsimprovegeneralpermissivenesstoantibioticresistanceplasmids