Tradeoff between lag time and growth rate drives the plasmid acquisition cost

Author(s)Ahmad, Mehrose
Author(s)Prensky, Hannah
Author(s)Balestrieri, Jacqueline
Author(s)ElNaggar, Shahd
Author(s)Gomez-Simmonds, Angela
Author(s)Uhlemann, Anne-Catrin
Author(s)Traxler, Beth
Author(s)Singh, Abhyudai
Author(s)Lopatkin, Allison J.
Date Accessioned2023-07-19T18:42:28Z
Date Available2023-07-19T18:42:28Z
Publication Date2023-04-24
DescriptionThis article was originally published in Nature Communications. The version of record is available at: https://doi.org/10.1038/s41467-023-38022-6. © The Author(s) 2023
AbstractConjugative plasmids drive genetic diversity and evolution in microbial populations. Despite their prevalence, plasmids can impose long-term fitness costs on their hosts, altering population structure, growth dynamics, and evolutionary outcomes. In addition to long-term fitness costs, acquiring a new plasmid introduces an immediate, short-term perturbation to the cell. However, due to the transient nature of this plasmid acquisition cost, a quantitative understanding of its physiological manifestations, overall magnitudes, and population-level implications, remains unclear. To address this, here we track growth of single colonies immediately following plasmid acquisition. We find that plasmid acquisition costs are primarily driven by changes in lag time, rather than growth rate, for nearly 60 conditions covering diverse plasmids, selection environments, and clinical strains/species. Surprisingly, for a costly plasmid, clones exhibiting longer lag times also achieve faster recovery growth rates, suggesting an evolutionary tradeoff. Modeling and experiments demonstrate that this tradeoff leads to counterintuitive ecological dynamics, whereby intermediate-cost plasmids outcompete both their low and high-cost counterparts. These results suggest that, unlike fitness costs, plasmid acquisition dynamics are not uniformly driven by minimizing growth disadvantages. Moreover, a lag/growth tradeoff has clear implications in predicting the ecological outcomes and intervention strategies of bacteria undergoing conjugation.
SponsorWe thank I. Gordo, D. Mazel, F. Dionisio, J. Alves Gama, E. Top, and M. Bruckner for their generous gifts (See Supplementary Methods). We also thank Maya Fabozzi from the Lopatkin Lab for generating the rifampicin-resistant mutant of the BW25113 strain. This study was funded by the National Science Foundation award #2040697 (A.J.L.) and the National Institute of Health awards #1R15GM143694-01 (A.J.L.) and #R01AI150152 (B.T.).
CitationAhmad, M., Prensky, H., Balestrieri, J. et al. Tradeoff between lag time and growth rate drives the plasmid acquisition cost. Nat Commun 14, 2343 (2023). https://doi.org/10.1038/s41467-023-38022-6
ISSN2041-1723
URLhttps://udspace.udel.edu/handle/19716/33023
Languageen_US
PublisherNature Communications
dc.rights.urihttp://creativecommons.org/licenses/by/4.0/
Keywordsmicrobial communities
Keywordspopulation dynamics
TitleTradeoff between lag time and growth rate drives the plasmid acquisition cost
TypeArticle
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