Signal diffusion and the mitigation of social exploitation in pneumococcal competence signalling

Abstract

Quorum sensing (QS) in bacteria is thought to enable populations of cells to coordinately and cooperatively regulate gene expression for traits that confer group benefits. While this view has strong empirical and theoretical support, it is increasingly appreciated that QS under natural conditions may be incapable of monitoring bacterial numbers and, furthermore, that QS is evolutionarily unstable owing to conflicts of interest among competing cells. An alternative hypothesis, termed diffusion sensing (DS), proposes that autoinducer secretion monitors the diffusive properties of the local environment, with benefits that are directly realized by individual cells rather than populations. Here, we test central predictions of this hypothesis using the competence signalling system of Streptococcus pneumoniae as our model, which regulates the induction of natural transformation by the secretion and detection of a small diffusible peptide, CSP (competence-stimulating peptide). By experimentally manipulating the diffusive properties of the growth medium, we found that there is no fixed quorum for competence induction. Instead, induction cell density scales with diffusivity. In agreement with QS and DS expectations, we show that the benefit of signal exploitation by mutant cells that can use but not secrete CSP is strongly frequency-dependent. However, we also find that the magnitude of this benefit declines significantly as diffusion is reduced, a result more consistent with the predictions of DS. Together, these data provide strong support for the DS hypothesis for autoinducer response systems. More specifically, our results imply that autonomous rather than group benefits should be sought in order to more completely understand the role and evolution of CSP signalling in pneumococci.

Cooperation, Quorum Sensing, and Evolution of Virulence in Staphylococcus aureus

“…1 and 2) (27). Although some previous studies are consistent with QS being a cooperative social trait, they have not shown the fitness benefit of responding to signal at the group level (5,40). Consequently, they are also consistent with a fitness benefit due to a nonsocial trait.…”

Spontaneous Gac Mutants of Pseudomonas Biological Control Strains: Cheaters or Mutualists?

“…This point parallels recent developments in the study of quorum-sensing signals. In natural settings, quorum-sensing signals may reach very high local con-centrations in even sparse populations when diffusion is restricted (7,10,17,37,48). Studies of quorum sensing conducted with liquid cultures tend to overestimate the relative importance of population size, because local increases in signal concentration are prevented.…”

Dynamics in the mixed microbial concourse

“…AgrA in turn activates a variety of virulence factors and enterotoxins (Lyon and Novick 2004). Peptide-based QS is employed by Bacillus subtilis and Streptococcus pneumoniae in the decision between competence and sporulation (Schultz et al 2009;Yang et al 2010). It has been postulated that signaling in these cases allows for coordinated population-level strategic bet hedging, with only a fraction of the population pursuing a potentially risky strategy like genetic competence (Dubnau and Losick 2006).…”