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

Mehrose Ahmad, Hannah Prensky, Jacqueline Balestrieri, Shahd ElNaggar, Angela Gomez-Simmonds, Anne-Catrin Uhlemann, Beth Traxler, Abhyudai Singh and Allison J. Lopatkin ()
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Mehrose Ahmad: Barnard College
Hannah Prensky: Barnard College
Jacqueline Balestrieri: Barnard College
Shahd ElNaggar: Barnard College
Angela Gomez-Simmonds: Columbia University Medical Center
Anne-Catrin Uhlemann: Columbia University Medical Center
Beth Traxler: University of Washington
Abhyudai Singh: University of Delaware
Allison J. Lopatkin: Barnard College

Nature Communications, 2023, vol. 14, issue 1, 1-12

Abstract: Abstract Conjugative 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.

Date: 2023
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DOI: 10.1038/s41467-023-38022-6

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