The fitness burden imposed by synthesising quorum sensing signals

Abstract

It is now well established that bacterial populations utilize cell-to-cell signaling (quorum-sensing, QS) to control the production of public goods and other co-operative behaviours. Evolutionary theory predicts that both the cost of signal production and the response to signals should incur fitness costs for producing cells. Although costs imposed by the downstream consequences of QS have been shown, the cost of QS signal molecule (QSSM) production and its impact on fitness has not been examined. We measured the fitness cost to cells of synthesising QSSMs by quantifying metabolite levels in the presence of QSSM synthases. We found that: (i) bacteria making certain QSSMs have a growth defect that exerts an evolutionary cost, (ii) production of QSSMs negatively correlates with intracellular concentrations of QSSM precursors, (iii) the production of heterologous QSSMs negatively impacts the production of a native QSSM that shares common substrates, and (iv) supplementation with exogenously added metabolites partially rescued growth defects imposed by QSSM synthesis. These data identify the sources of the fitness costs incurred by QSSM producer cells, and indicate that there may be metabolic trade-offs associated with QS signaling that could exert selection on how signaling evolves.

The Fitness of Pseudomonas aeruginosa Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment

“…However, when 10 µM exogenous 3O-C 12 -HSL was supplied, lasI mutants surpassed the wild type in growth (positive correlation between relative fitness and percent adenosine: coefficient, 8.74, P = 0.003) ( Fig. 2a and c ) This result is consistent with previous work demonstrating a cost to 3O-C 12 production ( 18 ). As predicted, this ability of lasI mutants to use exogenous signal, combined with the cost of signal production to the wild type, means that lasI mutants grown in coculture with wild-type bacteria act as social cheats: the average relative fitness was consistently >1 and did not decline as percent adenosine increased (coefficient, 1.8; P = 0.88) ( Fig.…”

“…However, little attention has been paid to whether QS signals themselves can act as exploitable public goods, despite there being a metabolic cost associated with the production of QS signals (even in the absence of downstream responses [ 18 , 19 ]). Previous experiments have shown that signal-negative mutants can act as cheats, but these were conducted under conditions where QS-dependent exoproducts enhance growth: these studies therefore do not separate the fitness effects of producing from those of responding to signal ( 5 , 6 ).…”

Peptide signaling without feedback in signal production operates as a true quorum sensing communication system in Bacillus subtilis

“…The variable peptide and isoprene moiety of ComX signaling molecule 19 enables this molecule to be intra-species specific 18 , 33 . High specificity has its price—our estimation of ComX molecule cost is 484 ATP, considerably more than 8 ATP for acyl-homoserine lactones (AHL) 29 based communication systems.…”

“…It was theoretically estimated that among SM, peptide signals of Gram-positive bacteria are more than 20 times metabolically more expensive than AHLs produced by Gram-negative bacteria 29 . The existence of fitness cost of signal molecule production in Gram-negative bacterial models has been theoretically predicted 30 – 32 and experimentally supported 33 . One would thus expect that the fitness burden of metabolically costly SM production in Gram-positives is even more pronounced.…”

Eavesdropping and crosstalk between secreted quorum sensing peptide signals that regulate bacteriocin production in Streptococcus pneumoniae

“…The four genotypes each release their own QS signal at equal concentrations (Table S2). Cells bind these secreted signals in a concentration dependent manner, at which point they are induced to produce bacteriocins that kill susceptible neighbor cells at the cost of reduced growth for the producer (Ruparell et al , 2016). While two faithful-signaling genotypes are only able to respond to their own signals, the two other eavesdropping genotypes can respond to multiple signals.…”