Quorum Sensing Signal Synthesis May Represent a Selective Advantage Independent of Its Role in Regulation of Bioluminescence in Vibrio fischeri

Grace Chong,Mike Manefield,Önder Kimyon,Eshel Ben-Jacob

doi:10.1371/journal.pone.0067443

Abstract

The evolution of biological signalling systems and apparently altruistic or cooperative traits in diverse organisms has required selection against the subversive tendencies of self-interested biological entities. The bacterial signalling and response system known as quorum sensing or Acylated Homoserine Lactone (AHL) mediated gene expression is thought to have evolved through kin selection. In this in vitro study on the model quorum sensing bioluminescent marine symbiont Vibrio fischeri, competition and long-term sub culturing experiments suggest that selection for AHL synthesis (encoded by the AHL synthase gene luxI) is independent of the quorum sensing regulated phenotype (bioluminescence encoded by luxCDABE). Whilst results support the hypothesis that signal response (AHL binding and transcriptional activation encoded by the luxR gene) is maintained through indirect fitness benefits (kin selection), signal synthesis is maintained in the V. fischeri genome over evolutionary time through direct fitness benefits at the individual level from an unknown function.

Highlights

The behaviour of biological systems requiring forms of signalling and cooperation between individual partner organisms have long garnered interest from evolutionary biologists [1]
It is generally believed that N-acyl-L-homoserine lactones (AHLs) are secondary metabolites that by definition play no role in cell-structure syntheses and energy transduction in the producer and are not essential for growth and reproductive metabolism [22]
We began our investigation seeking to confirm that deletion of the AHL synthase gene luxI did not compromise the ability of V. fischeri to reproduce by comparing growth of the wild type and its AHL synthase mutant in batch aerobic cultures in the presence and absence of the cognate AHL N-3-oxohexanoyl-L-homoserine lactone (OHHL) at 5 mM

Summary

Introduction

The behaviour of biological systems requiring forms of signalling and cooperation between individual partner organisms have long garnered interest from evolutionary biologists [1]. The interest generally stems from the challenge of explaining how cooperative traits resist corruption by the self-interest of partner individuals. The phenotypes regulated by quorum sensing are typically ecologically relevant only when expressed in concert by large populations of cells [6,7]. In this way both the concerted production of signalling molecules and the orchestrated expression of its regulated phenotypes are distinct cooperative traits that have survived the subversive tendencies of self-interested individuals over evolutionary time

Methods

Results

Conclusion