Abstract

Bacteria use a cell-cell communication system termed quorum-sensing (QS) to adjust population size by coordinating the costly but beneficial cooperative behaviors. It has long been suggested that bacterial social conflict for expensive extracellular products may drive QS divergence and cause the “tragedy of the commons”. However, the underlying molecular mechanism of social divergence and its evolutionary consequences for the bacterial ecology still remain largely unknown. By using the model bacterium Pseudomonas aeruginosa PAO1, here we show that nutrient reduction can promote QS divergence for population fitness during evolution but requiring adequate cell density. Mechanically, decreased nutrient supplies can induce RpoS-directed stringent response and enhance the selection pressure on lasR gene, and lasR mutants are evolved in association with the DNA mismatch repair “switch-off”. The lasR mutants have higher relative fitness than QS-intact individuals due to their energy-saving characteristic under nutrient decreased condition. Furthermore an optimal incorporation of lasR mutants is capable of maximizing the fitness of entire population during in vitro culture and the colonization in mouse lung. Consequently, rather than worsen the population health, QS-coordinated social divergence is an elaborate evolutionary strategy that renders the entire bacterial population more fit in tough times.

Highlights

  • To verify the idea that nutrient reduction may serve as selection pressure and promote the de novo emergence of QS-deficient individuals, we performed a series of long-term evolution of wild type (WT) PAO1 in QS-required and rich medium containing gradient concentrations of nutrient levels

  • Most of the previous evolutionary screenings of lasR mutants were performed in QS medium, and they concluded that lasR mutants can emerge under culture conditions that require QS-dependent extracellular products for growth[6,11,15]

  • We further extended this conclusion by culturing WT PAO1 in M9 medium containing gradient concentrations of caseinate with or without pre-added 3OC12-HSL, to investigate the relationship between nutrient supply and QS divergence

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Summary

Introduction

This result suggested that the time duration of QS divergence can be shortened with appropriately decreased nutrient supplies during evolution, as our screening and previous reports showed that lasR mutant would emerge after 10–15 days in 1% caseinate medium[6,11,21]. The total ATP productions of WT PAO1 and lasR mutant in the culture with gradient nutrient levels were measured to investigate the underlying mechanism of this growth divergence.

Results
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