Journal Article

Vertical and horizontal gene transfer tradeoffs direct plasmid fitness

Bethke, Jonathan H, Ma, Helena R, You, Lingchong, Xiao, Minfeng, Tsoi, Ryan, Cheng, Li

2023

Overview

Plasmid fitness is directed by two orthogonal processes—vertical transfer through cell division and horizontal transfer through conjugation. When considered individually, improvements in either mode of transfer can promote how well a plasmid spreads and persists. Together, however, the metabolic cost of conjugation could create a tradeoff that constrains plasmid evolution. Here, we present evidence for the presence, consequences, and molecular basis of a conjugation‐growth tradeoff across 40 plasmids derived from clinical Escherichia coli pathogens. We discover that most plasmids operate below a conjugation efficiency threshold for major growth effects, indicating strong natural selection for vertical transfer. Below this threshold, E. coli demonstrates a remarkable growth tolerance to over four orders of magnitude change in conjugation efficiency. This tolerance fades as nutrients become scarce and horizontal transfer attracts a greater share of host resources. Our results provide insight into evolutionary constraints directing plasmid fitness and strategies to combat the spread of antibiotic resistance. Synopsis Quantification of natural plasmid transfer rates reveals a tradeoff between conjugation and cell division that constrains plasmid evolution. Conjugation spreads multidrug‐resistant plasmids at a metabolic cost that can slow host growth. A wide range of conjugation efficiencies can be tolerated before incurring a transfer tradeoff. Intermediate conjugation efficiencies yield the highest plasmid abundance. Conjugation attracts a greater share of resources from nutrient‐starved hosts. Graphical Abstract Quantification of natural plasmid transfer rates reveals a tradeoff between conjugation and cell division that constrains plasmid evolution.

• Publisher: Nature Publishing Group UK,EMBO Press,John Wiley and Sons Inc,Springer Nature
• Subject: Anti-Bacterial Agents - pharmacology / Antibiotic resistance / Antibiotics / Cell division / Conjugation / Drug resistance / Drug Resistance, Microbial / E coli / Efficiency / EMBO16 / EMBO23 / Escherichia coli / Escherichia coli - genetics / Evolution / Fitness / Gene transfer / Gene Transfer, Horizontal / Genes / Horizontal cells / Horizontal transfer / Metabolism / Natural selection / Nutrients / Pathogens / plasmid / Plasmids / Plasmids - genetics / Reproductive fitness / resistance / tradeoff / Tradeoffs / Vertical transfer