Quorum sensing and the confusion about diffusion

West, Stuart A.; Winzer, Klaus; Gardner, Andy; Diggle, Stephen P.

doi:10.1016/j.tim.2012.09.004

Cited by 132 publications

(126 citation statements)

References 67 publications

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“…Despite detailed mechanistic understanding of the intracellular genetic architecture of QS, the functional roles of QS remain controversial (12,19). We propose a new functional model of "combinatorial QS" and demonstrate theoretically that bacteria can infer both their social (density) and physical (mass-transfer) environment, given combinatorial (nonadditive) responses to multiple signals with distinct half-lives.…”

Section: Discussionmentioning

confidence: 98%

“…Others have argued for a "diffusionsensing" interpretation, with more signal implying lower rates of mass transfer (diffusion or flow) (11). However, low mass transfer and high cellular density both lead to high signal concentrations, and so these two unknowns-information on the social parameter of cellular density and the asocial mass-transfer rate-are inextricably linked when only one signal is used (12,13). It is possible that a signal molecule can still provide a reliable indicator of the achievable density of a more costly secreted factor ("efficiency sensing") (13).…”

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confidence: 99%

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Combinatorial quorum sensing allows bacteria to resolve their social and physical environment

Cornforth

Popat

McNally

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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171

173

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Quorum sensing (QS) is a cell-cell communication system that controls gene expression in many bacterial species, mediated by diffusible signal molecules. Although the intracellular regulatory mechanisms of QS are often well-understood, the functional roles of QS remain controversial. In particular, the use of multiple signals by many bacterial species poses a serious challenge to current functional theories. Here, we address this challenge by showing that bacteria can use multiple QS signals to infer both their social (density) and physical (mass-transfer) environment. Analytical and evolutionary simulation models show that the detection of, and response to, complex social/physical contrasts requires multiple signals with distinct half-lives and combinatorial (nonadditive) responses to signal concentrations. We test these predictions using the opportunistic pathogen Pseudomonas aeruginosa and demonstrate significant differences in signal decay between its two primary signal molecules, as well as diverse combinatorial responses to dual-signal inputs. QS is associated with the control of secreted factors, and we show that secretome genes are preferentially controlled by synergistic "AND-gate" responses to multiple signal inputs, ensuring the effective expression of secreted factors in high-density and low mass-transfer environments. Our results support a new functional hypothesis for the use of multiple signals and, more generally, show that bacteria are capable of combinatorial communication.diffusion sensing | bacterial signaling | efficiency sensing | collective behavior | bacterial cooperation

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Section: Discussionmentioning

confidence: 98%

mentioning

confidence: 99%

Combinatorial quorum sensing allows bacteria to resolve their social and physical environment

Cornforth

Popat

McNally

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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171

173

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“…As a result, several new phenomena emerge due to crosstalk between spatially segregated populations [6]. Consequently, it appears that AI molecules can be an indicator of increased local population density, and can also be proxies of other variables, such as population dispersal [7][8][9][10][11].In recent years, advances in the ability to experimentally probe the properties of cellular populations at the single-cell level [12] have resulted in a growing community of theoretical physicists working to catalogue the different classes of collective behavior found in interacting communities of organisms [13][14][15][16][17]. This approach has already successfully yielded insight into a wide variety of ecological problems, with notable recent examples including the effects of invasion in cooperative populations [18], optimal foraging strategies in sheep herds [19], and the properties of microbial signal transduction net-…”

mentioning

confidence: 99%

mentioning

confidence: 99%

Spatial dispersal of bacterial colonies induces a dynamical transition from local to global quorum sensing

Yusufaly

Boedicker

2016

Phys. Rev. E

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Bacteria communicate using external chemical signals called autoinducers (AI) in a process known as quorum sensing (QS). QS efficiency is reduced by both limitations of AI diffusion and potential interference from neighboring strains. There is thus a need for predictive theories of how spatial community structure shapes information processing in complex microbial ecosystems. As a step in this direction, we apply a reaction-diffusion model to study autoinducer signaling dynamics in a single-species community as a function of the spatial distribution of colonies in the system. We predict a dynamical transition between a local quorum sensing (LQS) regime, with the AI signaling dynamics primarily controlled by the local population densities of individual colonies, and a global quorum sensing (GQS) regime, with the dynamics being dependent on collective intercolony diffusive interactions. The crossover between LQS to GQS is intimately connected to a tradeoff between the signaling network's latency, or speed of activation, and its throughput, or the total spatial range over which all the components of the system communicate.Multicellular communities, such as colonies of bacteria, communicate with each other to coordinate changes in their collective group behavior. This communication usually takes the form of the production and secretion of extracellular signaling molecules called autoinducers (AI), as illustrated in Figure 1. Released autoinducers diffuse through the environment, and each cell senses the local concentration of signal to inform changes in gene regulation. This intercellular signaling network, known as quorum sensing (QS), is crucial for a wide array of important microbial processes, including biofilm formation, regulation of virulence and horizontal gene transfer [1][2][3].Decades of research have advanced our knowledge of QS, but several subtleties remain unresolved. In particular, AI signals may convey information about many aspects of the cellular network and local environment beyond simply the total number of cells in the system [4]. Far from being reducible to homogeneous, uniform density populations, microbial communities are typically characterized by high spatial heterogeneity [5]. As a result, several new phenomena emerge due to crosstalk between spatially segregated populations [6]. Consequently, it appears that AI molecules can be an indicator of increased local population density, and can also be proxies of other variables, such as population dispersal [7][8][9][10][11].In recent years, advances in the ability to experimentally probe the properties of cellular populations at the single-cell level [12] have resulted in a growing community of theoretical physicists working to catalogue the different classes of collective behavior found in interacting communities of organisms [13][14][15][16][17]. This approach has already successfully yielded insight into a wide variety of ecological problems, with notable recent examples including the effects of invasion in cooperative populations [18], opti...

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“…The spatial distribution of bacteria affects the activation of a QS switch (27). The concentration of a signaling molecule diminishes as it moves away from a cell, which decreases the likelihood of activating the QS switch (28).…”

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confidence: 99%

Quorum-sensing Salmonella selectively trigger protein expression within tumors

Swofford

Dessel

Forbes

2015

Proc. Natl. Acad. Sci. U.S.A.

106

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Salmonella that secrete anticancer proteins have the potential to eliminate tumors, but nonspecific expression causes damage to healthy tissue. We hypothesize that Salmonella, integrated with a density-dependent switch, would only express proteins in tightly packed colonies within tumors. To test this hypothesis, we cloned the lux quorum-sensing (QS) system and a GFP reporter into nonpathogenic Salmonella. Fluorescence and bacterial density were measured in culture and in a tumor-on-a-chip device to determine the critical density necessary to initiate expression. QS Salmonella were injected into 4T1 tumor-bearing mice to quantify GFP expression in vivo using immunofluorescence. At densities below 0.6 × 1010 cfu/g in tumors, less than 3% of QS Salmonella expressed GFP. Above densities of 4.2 × 1010 cfu/g, QS Salmonella had similar expression levels to constitutive controls. GFP expression by QS colonies was dependent upon the distance to neighboring bacteria. No colonies expressed GFP when the average distance to neighbors was greater than 155 µm. Calculations of autoinducer concentrations showed that expression was sigmoidally dependent on density and inversely dependent on average radial distance. Based on bacterial counts from excised tissue, the liver density (0.0079 × 1010 cfu/g) was less than the critical density (0.11 × 1010 cfu/g) necessary to initiate expression. QS Salmonella are a promising tool for cancer treatment that will target drugs to tumors while preventing damage to healthy tissue.

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Quorum sensing and the confusion about diffusion

Cited by 132 publications

References 67 publications

Combinatorial quorum sensing allows bacteria to resolve their social and physical environment

Combinatorial quorum sensing allows bacteria to resolve their social and physical environment

Spatial dispersal of bacterial colonies induces a dynamical transition from local to global quorum sensing

Quorum-sensing Salmonella selectively trigger protein expression within tumors

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