Ratiometric quorum sensing governs the trade-off between bacterial vertical and horizontal antibiotic resistance propagation

Plasmid-mediated horizontal gene transfer of antibiotic resistance and virulence in pathogenic bacteria underlies a major public health issue. Understanding how, in the absence of antibiotic-mediated selection, plasmid-bearing cells avoid being outnumbered by plasmid-free cells is key to developing...

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Bibliographic Details
Published in:PLoS biology 2020-08, Vol.18 (8), p.e3000814-e3000814
Main Authors: Banderas, Alvaro, Carcano, Arthur, Sia, Elisa, Li, Shuang, Lindner, Ariel B, Roberts, Roland G
Format: Article
Language:English
Subjects:
Antibiotic resistance
Antibiotics
Bacteria
Bacteria, Pathogenic
Bacteriology
Binding sites
Biodiversity
Biology and Life Sciences
Conjugation
Drug resistance
Drug resistance in microorganisms
Engineering
Flow cytometry
Gene expression
Gene transfer
Genetic aspects
Genetic transformation
Gram-positive bacteria
Growth rate
Horizontal transfer
Life Sciences
Mathematical models
Mating
Medicine and Health Sciences
Microbiology and Parasitology
Observations
Pheromones
Physiological aspects
Plasmids
Population
Population number
Populations and Evolution
Proteins
Public health
Quorum sensing
Robustness (mathematics)
Sex pheromone
Short Reports
Social Sciences
Virulence
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Summary:Plasmid-mediated horizontal gene transfer of antibiotic resistance and virulence in pathogenic bacteria underlies a major public health issue. Understanding how, in the absence of antibiotic-mediated selection, plasmid-bearing cells avoid being outnumbered by plasmid-free cells is key to developing counterstrategies. Here, we quantified the induction of the plasmidial sex pheromone pathway of Enterococcus faecalis to show that the integration of the stimulatory (mate-sensing) and inhibitory (self-sensing) signaling modules from the pCF10 conjugative plasmid provides a precise measure of the recipient-to-donor ratio, agnostic to variations in population size. Such ratiometric control of conjugation favors vertical plasmid transfer under low mating likelihood and allows activation of conjugation functions only under high mating likelihood. We further show that this strategy constitutes a cost-effective investment into mating effort because overstimulation produces unproductive self-aggregation and growth rate reduction. A mathematical model suggests that ratiometric control of conjugation increases plasmid fitness and predicts a robust long-term, stable coexistence of donors and recipients. Our results demonstrate how population-level parameters can control transfer of antibiotic resistance in bacteria, opening the door for biotic control strategies.
ISSN:1545-7885
1544-9173
1545-7885
DOI:10.1371/journal.pbio.3000814