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Effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis

BACKGROUND: Conjugation plays a major role in the transmission of plasmids encoding antibiotic resistance genes in both clinical and general settings. The conjugation efficiency is influenced by many biotic and abiotic factors, one of which is the taxonomic relatedness between donor and recipient ba...

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Autores principales: Alderliesten, Jesse B., Duxbury, Sarah J. N., Zwart, Mark P., de Visser, J. Arjan G. M., Stegeman, Arjan, Fischer, Egil A. J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7249681/
https://www.ncbi.nlm.nih.gov/pubmed/32456625
http://dx.doi.org/10.1186/s12866-020-01825-4
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author Alderliesten, Jesse B.
Duxbury, Sarah J. N.
Zwart, Mark P.
de Visser, J. Arjan G. M.
Stegeman, Arjan
Fischer, Egil A. J.
author_facet Alderliesten, Jesse B.
Duxbury, Sarah J. N.
Zwart, Mark P.
de Visser, J. Arjan G. M.
Stegeman, Arjan
Fischer, Egil A. J.
author_sort Alderliesten, Jesse B.
collection PubMed
description BACKGROUND: Conjugation plays a major role in the transmission of plasmids encoding antibiotic resistance genes in both clinical and general settings. The conjugation efficiency is influenced by many biotic and abiotic factors, one of which is the taxonomic relatedness between donor and recipient bacteria. A comprehensive overview of the influence of donor-recipient relatedness on conjugation is still lacking, but such an overview is important to quantitatively assess the risk of plasmid transfer and the effect of interventions which limit the spread of antibiotic resistance, and to obtain parameter values for conjugation in mathematical models. Therefore, we performed a meta-analysis on reported conjugation frequencies from Escherichia coli donors to various recipient species. RESULTS: Thirty-two studies reporting 313 conjugation frequencies for liquid broth matings and 270 conjugation frequencies for filter matings were included in our meta-analysis. The reported conjugation frequencies varied over 11 orders of magnitude. Decreasing taxonomic relatedness between donor and recipient bacteria, when adjusted for confounding factors, was associated with a lower conjugation frequency in liquid matings. The mean conjugation frequency for bacteria of the same order, the same class, and other classes was 10, 20, and 789 times lower than the mean conjugation frequency within the same species, respectively. This association between relatedness and conjugation frequency was not found for filter matings. The conjugation frequency was furthermore found to be influenced by temperature in both types of mating experiments, and in addition by plasmid incompatibility group in liquid matings, and by recipient origin and mating time in filter matings. CONCLUSIONS: In our meta-analysis, taxonomic relatedness is limiting conjugation in liquid matings, but not in filter matings, suggesting that taxonomic relatedness is not a limiting factor for conjugation in environments where bacteria are fixed in space.
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spelling pubmed-72496812020-06-04 Effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis Alderliesten, Jesse B. Duxbury, Sarah J. N. Zwart, Mark P. de Visser, J. Arjan G. M. Stegeman, Arjan Fischer, Egil A. J. BMC Microbiol Research Article BACKGROUND: Conjugation plays a major role in the transmission of plasmids encoding antibiotic resistance genes in both clinical and general settings. The conjugation efficiency is influenced by many biotic and abiotic factors, one of which is the taxonomic relatedness between donor and recipient bacteria. A comprehensive overview of the influence of donor-recipient relatedness on conjugation is still lacking, but such an overview is important to quantitatively assess the risk of plasmid transfer and the effect of interventions which limit the spread of antibiotic resistance, and to obtain parameter values for conjugation in mathematical models. Therefore, we performed a meta-analysis on reported conjugation frequencies from Escherichia coli donors to various recipient species. RESULTS: Thirty-two studies reporting 313 conjugation frequencies for liquid broth matings and 270 conjugation frequencies for filter matings were included in our meta-analysis. The reported conjugation frequencies varied over 11 orders of magnitude. Decreasing taxonomic relatedness between donor and recipient bacteria, when adjusted for confounding factors, was associated with a lower conjugation frequency in liquid matings. The mean conjugation frequency for bacteria of the same order, the same class, and other classes was 10, 20, and 789 times lower than the mean conjugation frequency within the same species, respectively. This association between relatedness and conjugation frequency was not found for filter matings. The conjugation frequency was furthermore found to be influenced by temperature in both types of mating experiments, and in addition by plasmid incompatibility group in liquid matings, and by recipient origin and mating time in filter matings. CONCLUSIONS: In our meta-analysis, taxonomic relatedness is limiting conjugation in liquid matings, but not in filter matings, suggesting that taxonomic relatedness is not a limiting factor for conjugation in environments where bacteria are fixed in space. BioMed Central 2020-05-26 /pmc/articles/PMC7249681/ /pubmed/32456625 http://dx.doi.org/10.1186/s12866-020-01825-4 Text en © The Author(s) 2020 Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Alderliesten, Jesse B.
Duxbury, Sarah J. N.
Zwart, Mark P.
de Visser, J. Arjan G. M.
Stegeman, Arjan
Fischer, Egil A. J.
Effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis
title Effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis
title_full Effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis
title_fullStr Effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis
title_full_unstemmed Effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis
title_short Effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis
title_sort effect of donor-recipient relatedness on the plasmid conjugation frequency: a meta-analysis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7249681/
https://www.ncbi.nlm.nih.gov/pubmed/32456625
http://dx.doi.org/10.1186/s12866-020-01825-4
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