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Abstract Plasmids are autonomous genetic elements that can be exchanged between microorganisms via horizontal gene transfer (HGT). Despite the central role they play in antibiotic resistance and modern biotechnology, our understanding of plasmids’ natural ecology is limited. Recent experiments have shown that plasmids can spread even when they are a burden to the cell, suggesting that natural plasmids may exist as parasites. Here, we use mathematical modeling to explore the ecology of such parasitic plasmids. We first develop models of single plasmids and find that a plasmid’s population dynamics and optimal infection strategy are strongly determined by the plasmid’s HGT mechanism. We then analyze models of co-infecting plasmids and show that parasitic plasmids are prone to a “tragedy of the commons” in which runaway plasmid invasion severely reduces host fitness. We propose that this tragedy of the commons is averted by selection between competing populations and demonstrate this effect in a metapopulation model. We derive predicted distributions of unique plasmid types in genomes—comparison to the distribution of plasmids in a collection of 17,725 genomes supports a model of parasitic plasmids with positive plasmid–plasmid interactions that ameliorate plasmid fitness costs or promote the invasion of new plasmids.
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Tradeoff between lag time and growth rate drives the plasmid acquisition cost
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.
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- Award ID(s):
- 2040697
- PAR ID:
- 10408708
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 14
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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