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

Jesse B Alderliesten,Sarah J N Duxbury,Mark P Zwart,J Arjan G M De Visser,Arjan Stegeman,Egil A J Fischer

doi:10.1186/s12866-020-01825-4

Jesse B Alderliesten, Sarah J N Duxbury + Show 4 more

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https://doi.org/10.1186/s12866-020-01825-4

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Abstract

BackgroundConjugation 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.ResultsThirty-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.ConclusionsIn 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.

Highlights

Conjugation plays a major role in the transmission of plasmids encoding antibiotic resistance genes in both clinical and general settings
A key factor in the spread of Antibiotic resistance (ABR) is the transmission of plasmids that encode ABR genes [4], which is the focus of this review
Identification of relevant studies Our selection for studies which mentioned more than one recipient species in the abstract, used liquid broth matings or filter matings with E. coli donors containing a self-transmissible plasmid yielded 32 studies (Fig. 1)

Summary

Introduction

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. Antibiotic resistance (ABR) in bacteria is recognised world-wide as an important threat to human and animal health [1,2,3]. To address this threat, a better understanding of the key factors that determine the spread of ABR between bacteria is needed. The major role of conjugation in the spread of ABR genes in both clinical and general settings is evident [5,6,7]

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