Environmental modification via a quorum sensing molecule influences the social landscape of siderophore production.

Roman Popat,Ana C Da Silva,Scott A S Easton,Luke Mcnally,Paul Williams,Stephen P Diggle,Freya Harrison

doi:10.1098/rspb.2017.0200

Abstract

Bacteria produce a wide variety of exoproducts that favourably modify their environment and increase their fitness. These are often termed ‘public goods’ because they are costly for individuals to produce and can be exploited by non-producers (cheats). The outcome of conflict over public goods is dependent upon the prevailing environment and the phenotype of the individuals in competition. Many bacterial species use quorum sensing (QS) signalling molecules to regulate the production of public goods. QS, therefore, determines the cooperative phenotype of individuals, and influences conflict over public goods. In addition to their regulatory functions, many QS molecules have additional properties that directly modify the prevailing environment. This leads to the possibility that QS molecules could influence conflict over public goods indirectly through non-signalling effects, and the impact of this on social competition has not previously been explored. The Pseudomonas aeruginosa QS signal molecule PQS is a powerful chelator of iron which can cause an iron starvation response. Here, we show that PQS stimulates a concentration-dependent increase in the cooperative production of iron scavenging siderophores, resulting in an increase in the relative fitness of non-producing siderophore cheats. This is likely due to an increased cost of siderophore output by producing cells and a concurrent increase in the shared benefits, which accrue to both producers and cheats. Although PQS can be a beneficial signalling molecule for P. aeruginosa, our data suggest that it can also render a siderophore-producing population vulnerable to competition from cheating strains. More generally, our results indicate that the production of one social trait can indirectly affect the costs and benefits of another social trait.

Highlights

Bacterial cells secrete numerous extracellular factors to favourably modify their environment
We show that the iron-chelating properties of pseudomonas quinolone signal (PQS) lead to increased production of costly siderophores and increased relative fitness of a siderophore cheat
We found that the addition of synthetic PQS to cultures of P. aeruginosa results in a concentration-dependent decrease in bacterial fitness and an increase in the production of the siderophores pyoverdine and pyochelin

Summary

Introduction

Bacterial cells secrete numerous extracellular factors to favourably modify their environment. Cells produce and release QS molecules to regulate the production of a range of public goods which aid in scavenging for nutrients, providing scaffolding for biofilms and facilitating motility Because these cooperative secretions can be key determinants of successful growth or persistence, there has been considerable interest in the impact of QS on ecological competition between different genotypes or strains of bacteria [7,8,9]. We pre-cultured, washed and density corrected both strains and mixed them to a ratio of approximately 99 : 1 (producer : nonproducer) We incubated these in 5 ml iron-limited medium (CAA) in the presence and absence of 50 mM PQS for 24 h at 378C with agitation at 200 r.p.m. To measure relative abundance of the strains, we plated the co-cultures before and after incubation, and counted total colonies and luminescent colonies. We conclude that it is the iron-chelating activity of PQS, and not its signal function, that triggers an iron starvation response: cells increase their production of iron scavenging siderophores and either a metabolic burden or slower uptake due to the presence of a chelator leads to poorer growth

Results

Discussion