Ecological feedback in quorum-sensing microbial populations can induce heterogeneous production of autoinducers

Bauer, Matthias; Knebel, Johannes; Lechner, Matthias; Pickl, Peter; Frey, Erwin

doi:10.7554/elife.25773

Cited by 33 publications

(43 citation statements)

References 95 publications

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“…Maintaining phenotypic heterogeneity in HCD quorum-sensing populations could allow the bacteria to undertake bet-hedging 59 strategies in which, simultaneously, some cells in the population perform individual behaviours whereas others engage in collective activities. Consistent with this idea, modelling efforts suggest that bacteria alter their immediate surroundings by secreting autoinducers and that they respond to their local environment by increasing the rate of autoinducer production, setting up a positive feedback loop that ensures that autoinducers are produced by only a regional subpopulation of cells 60 . This model proposes that heterogeneity arises from a balance between the fitness advantage gained by the nonproducers who avoid the costly production of autoinducers and the persistence of producers that engage in the autoinduction loop, ultimately allowing separate subpopulations to coexist.…”

Section: Heterogeneity In Quorum Sensingmentioning

confidence: 94%

Bacterial quorum sensing in complex and dynamically changing environments

2019

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Quorum sensing is a process of bacterial cell-to-cell chemical communication that relies on the production, detection and response to extracellular signalling molecules called autoinducers. Quorum sensing allows groups of bacteria to synchronously alter behaviour in response to changes in the population density and species composition of the vicinal community. Quorum-sensingmediated communication is now understood to be the norm in the bacterial world. Elegant research has defined quorum-sensing components and their interactions, for the most part, under ideal and highly controlled conditions. Indeed, these seminal studies laid the foundations for the field. In this Review, we highlight new findings concerning how bacteria deploy quorum sensing in realistic scenarios that mimic nature. We focus on how quorums are detected and how quorum sensing controls group behaviours in complex and dynamically changing environments such as multi-species bacterial communities, in the presence of flow, in 3D non-uniform biofilms and in hosts during infection. Bacteria, once thought capable of only simple processes and single-celled life, are now appreciated for their ability to act collectively in multi-cellular groups 1,2. Coordinated behaviours include bioluminescence 3,4 , virulence factor production 5,6 , secondary metabolite

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Section: Heterogeneity In Quorum Sensingmentioning

confidence: 94%

Bacterial quorum sensing in complex and dynamically changing environments

2019

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“…S14, Movie 17-19) . The higher-than-basal levels of AI produced by the induced subpopulation could be key to the maintenance of the high stable state of expression of QS genes 37,38 in the presence of active environmental suppression. Indeed, simultaneous induction and repression with exogenous AI and glucose, respectively, stably maintained an induced subpopulation (Fig.…”

Section: Resultsmentioning

confidence: 99%

Environmental sensing in dynamic quorum responses

Chu

Groisman²,

Levchenko

2019

Preprint

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14Cell communication and coordinated cell behavior are hallmarks of multicellular behavior of 15 living systems. However, in many cases, including the ancient and archetypal example of 16 bacterial quorum sensing, the meaning of the communicated information remains a subject of 17 debate. It is commonly assumed that quorum sensing encodes the information on the current 18 state of the colony, including cell density and physical colony confinement. Here, we show that 19 quorum sensing can also be exquisitely sensitive to dynamic changes in the environment, 20including fluctuations of the prevailing nutrient source. We propose a new signaling mechanism 21 accounting for this sensory capability. This mechanism combines regulation by the commonly 22 studied lux operon-encoded network with the environmentally determined balance of protein 23 synthesis and dilution rates, dependent on the rate of cell proliferation. This regulatory 24 mechanism accounts for observed complex spatial distribution of quorum responses, and 25 emergence of sophisticated processing of dynamic inputs, including temporal thresholds and 26 persistent partial induction following a transient change in the environmental conditions. We 27 further show that, in this context, cell communication in quorum sensing acquires a new 28 meaning: education of cells within a population about the past history of transient exposure to 29 adverse conditions by a subset of induced cells. In combination, these signaling and 30 communication features may endow a cell population with increased fitness in diverse 31 fluctuating environments. 32 33 high cell density might also hamper nutrient availability 22 ; however, neither CD nor DF sensing 51 interpretations directly relate to the detection of changes in the environmental conditions, 52 particularly of subtle fluctuations in nutrient content. It is not clear, therefore, whether QS might 53in fact be a mechanism to sense dynamic changes in the potentially stressful, dynamic cell 54 microenvironment 23 , or it just enables this sensing (e.g., in a cell density-dependent fashion) 55 through alternative sensory mechanisms 24 . 56 3 57To explore the function of QS, it is important to investigate the dynamic features of QS 58 responses. However, the emphasis has traditionally been placed on the categorical on or off 59 description, stemming from the common feature of the molecular circuits underlying QS -the 60 positive feedback. Positive autoregulation is observed, for example, in a frequently studied QS 61 circuit of the marine bacterium V. fischeri, whose response is controlled by the lux operon 25 . It 62 involves AI, produced by the AI synthase LuxI, binding to its cognate cytoplasmic AI receptor 63LuxR, and positively auto-regulating the LuxI and LuxR in addition to driving bioluminescence 64 gene transcription 26-28 . This simple feedback regulatory circuit enables a switch-like increase in 65 the QS response after the threshold concentration of AI is exceeded 29 . However, the time scale of 66 this response and...

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“…So accounting for regulation, which has been shown to also impact growth [65], will also necessarily involve elaborate produc-tion curves [63] and cost-saving strategies [66]. Ultimately, adaptive production raises complex questions about how cells shape the ecological and environmental conditions in which they interact [67]. Another possible extension would be to allow privatized use of the public good.…”

Section: Discussionmentioning

confidence: 99%

Interactions mediated by a public good transiently increase cooperativity in growing Pseudomonas putida metapopulations

Becker

Wienand

Lechner

et al. 2018

Sci Rep

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Bacterial communities have rich social lives. A well-established interaction involves the exchange of a public good in Pseudomonas populations, where the iron-scavenging compound pyoverdine, synthesized by some cells, is shared with the rest. Pyoverdine thus mediates interactions between producers and non-producers and can constitute a public good. This interaction is often used to test game theoretical predictions on the “social dilemma” of producers. Such an approach, however, underestimates the impact of specific properties of the public good, for example consequences of its accumulation in the environment. Here, we experimentally quantify costs and benefits of pyoverdine production in a specific environment, and build a model of population dynamics that explicitly accounts for the changing significance of accumulating pyoverdine as chemical mediator of social interactions. The model predicts that, in an ensemble of growing populations (metapopulation) with different initial producer fractions (and consequently pyoverdine contents), the global producer fraction initially increases. Because the benefit of pyoverdine declines at saturating concentrations, the increase need only be transient. Confirmed by experiments on metapopulations, our results show how a changing benefit of a public good can shape social interactions in a bacterial population.

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Ecological feedback in quorum-sensing microbial populations can induce heterogeneous production of autoinducers

Cited by 33 publications

References 95 publications

Bacterial quorum sensing in complex and dynamically changing environments

Bacterial quorum sensing in complex and dynamically changing environments

Environmental sensing in dynamic quorum responses

Interactions mediated by a public good transiently increase cooperativity in growing Pseudomonas putida metapopulations

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