Bacterium in a box: sensing of quorum and environment by the LuxI/LuxR gene regulatory circuit

Hagen, Stephen J.; Son, Minjun; Weiss, Joel T.; Young, Jonathan H.

doi:10.1007/s10867-010-9186-4

Cited by 19 publications

(9 citation statements)

References 18 publications

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“…The heterogeneity observed here may also argue against an interpretation of the LuxI/LuxR system – or at least its regulation of the bioluminescence genes – as allowing an individual cell to acquire much useful information about its local microenvironment [4] , [5] , [36] . The individual luminescence response seems to contain little information about ( i.e.…”

Section: Discussionmentioning

confidence: 90%

Heterogeneous Response to a Quorum-Sensing Signal in the Luminescence of Individual Vibrio fischeri

Pérez

Hagen

2010

PLoS ONE

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The marine bacterium Vibrio fischeri regulates its bioluminescence through a quorum sensing mechanism: the bacterium releases diffusible small molecules (autoinducers) that accumulate in the environment as the population density increases. This accumulation of autoinducer (AI) eventually activates transcriptional regulators for bioluminescence as well as host colonization behaviors. Although V.fischeri quorum sensing has been extensively characterized in bulk populations, far less is known about how it performs at the level of the individual cell, where biochemical noise is likely to limit the precision of luminescence regulation. We have measured the time-dependence and AI-dependence of light production by individual V.fischeri cells that are immobilized in a perfusion chamber and supplied with a defined concentration of exogenous AI. We use low-light level microscopy to record and quantify the photon emission from the cells over periods of several hours as they respond to the introduction of AI. We observe an extremely heterogeneous response to the AI signal. Individual cells differ widely in the onset time for their luminescence and in their resulting brightness, even in the presence of high AI concentrations that saturate the light output from a bulk population. The observed heterogeneity shows that although a given concentration of quorum signal may determine the average light output from a population of cells, it provides far weaker control over the luminescence output of each individual cell.

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Section: Discussionmentioning

confidence: 90%

Heterogeneous Response to a Quorum-Sensing Signal in the Luminescence of Individual Vibrio fischeri

Pérez

Hagen

2010

PLoS ONE

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“…S1 in the supplemental material). PCR amplification using the primer set P luxI (5=-GGTACCACCTGTAGGATCGTACAGGT-3=) and P luxR (5=-GAATTCTTAATTTTTAAAGTATGGGCAATCAATTG-3=) including additional restriction sites (sequences are underlined) and genomic DNA from V. fischeri (DSM 2168) amplified a 977-bp fragment comprising the V. fischeri luxRI gene, including the promoter of the lux operon (59,60) and additional restriction sites for KpnI at the 5= end and for EcoRI at the 3= end. PCR amplification with the primer set P lsrAfor (5=-GGTACCCGC GACCTGTTCTTCTT-3=) and P lsrArev (5=-GAATTCCATATTTCCCCCG TTCAGTT-3=) and genomic DNA from E. coli K-12 MG1655 produced the 319-bp E. coli lsrA promoter region (11) containing additional 5= KpnI and 3= EcoRI restriction sites.…”

Section: Methodsmentioning

confidence: 99%

Novel Reporter for Identification of Interference with Acyl Homoserine Lactone and Autoinducer-2 Quorum Sensing

Weiland‐Bräuer

Pinnow

Schmitz

2015

Appl Environ Microbiol

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Two reporter strains were established to identify novel biomolecules interfering with bacterial communication (quorum sensing [QS]). The basic design of these Escherichia coli-based systems comprises a gene encoding a lethal protein fused to promoters induced in the presence of QS signal molecules. Consequently, these E. coli strains are unable to grow in the presence of the respective QS signal molecules unless a nontoxic QS-interfering compound is present. The first reporter strain designed to detect autoinducer-2 (AI-2)-interfering activities (AI2-QQ.1) contained the E. coli ccdB lethal gene under the control of the E. coli lsrA promoter. The second reporter strain (AI1-QQ.1) contained the Vibrio fischeri luxI promoter fused to the ccdB gene to detect interference with acyl-homoserine lactones. Bacteria isolated from the surfaces of several marine eukarya were screened for quorum-quenching (QQ) activities using the established reporter systems AI1-QQ.1 and AI2-QQ.1. Out of 34 isolates, two interfered with acylated homoserine lactone (AHL) signaling, five interfered with AI-2 QS signaling, and 10 were demonstrated to interfere with both signal molecules. Open reading frames (ORFs) conferring QQ activity were identified for three selected isolates (Photobacterium sp., Pseudoalteromonas sp., and Vibrio parahaemolyticus). Evaluation of the respective heterologously expressed and purified QQ proteins confirmed their ability to interfere with the AHL and AI-2 signaling processes. Q uorum sensing (QS) is the cell-cell communication betweenbacteria that allows the perception of population density by small signaling molecules-so-called autoinducers-and modifies gene expression in response to the population density. It controls a wide spectrum of processes and phenotypic behaviors, including stress resistance, production of toxins and secondary metabolites, pathogenicity, swarming, and biofilm formation (for a review, see references 1 and 2). In addition to playing important roles in intraspecies and interspecies communication, QS is also involved in host-microbe interactions (3-5). Intraspecific communication of Gram-negative bacteria is based on the production and perception of acylated homoserine lactones (AHLs) synthesized by LuxI homologs. Increasing intracellular concentrations of diffusible AHLs with higher cell densities are perceived by binding of the AHLs to the cognate receptor (e.g., LuxR in Vibrio fischeri), resulting in activation or inhibition of target gene transcription (6, 7). Interspecific communication between different species within one habitat has been demonstrated to depend on the synthesis and detection of the universal autoinducer-2 (AI-2), which can be inhibited by furanones (8, 9). The perception of these signal molecules is achieved either by a two-component regulatory system (e.g., in Vibrio harveyi, where the induced phosphorylation cascade finally results in the induction of specific target genes) (10), or by transportation of the signal molecule into the cell (e.g., in Escherichia coli,...

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“…However, how individual cells behave remains puzzling. In fact, as observed in Vibrio harveyi [12], Vibrio fischeri [13], Pseudomonas aeruginosa [14], and luxI / luxR-GFP strains of E. coli [15], the cellular response to QS signals seems to be highly heterogeneous at the level of the distribution of both the population phenotype and the response times of individual cells.…”

Section: Introductionmentioning

confidence: 99%

Dynamics of the quorum sensing switch: stochastic and non-stationary effects

Weber¹,

Buceta²

2013

BMC Syst Biol

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Background: A wide range of bacteria species are known to communicate through the so called quorum sensing (QS) mechanism by means of which they produce a small molecule that can freely diffuse in the environment and in the cells. Upon reaching a threshold concentration, the signalling molecule activates the QS-controlled genes that promote phenotypic changes. This mechanism, for its simplicity, has become the model system for studying the emergence of a global response in prokaryotic cells. Yet, how cells precisely measure the signal concentration and act coordinately, despite the presence of fluctuations that unavoidably affects cell regulation and signalling, remains unclear. Results: We propose a model for the QS signalling mechanism in Vibrio fischeri based on the synthetic strains lux01 and lux02. Our approach takes into account the key regulatory interactions between LuxR and LuxI, the autoinducer transport, the cellular growth and the division dynamics. By using both deterministic and stochastic models, we analyze the response and dynamics at the single-cell level and compare them to the global response at the population level. Our results show how fluctuations interfere with the synchronization of the cell activation and lead to a bimodal phenotypic distribution. In this context, we introduce the concept of precision in order to characterize the reliability of the QS communication process in the colony. We show that increasing the noise in the expression of LuxR helps cells to get activated at lower autoinducer concentrations but, at the same time, slows down the global response. The precision of the QS switch under non-stationary conditions decreases with noise, while at steady-state it is independent of the noise value. Conclusions:Our in silico experiments show that the response of the LuxR/LuxI system depends on the interplay between non-stationary and stochastic effects and that the burst size of the transcription/translation noise at the level of LuxR controls the phenotypic variability of the population. These results, together with recent experimental evidences on LuxR regulation in wild-type species, suggest that bacteria have evolved mechanisms to regulate the intensity of those fluctuations.

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Bacterium in a box: sensing of quorum and environment by the LuxI/LuxR gene regulatory circuit

Cited by 19 publications

References 18 publications

Heterogeneous Response to a Quorum-Sensing Signal in the Luminescence of Individual Vibrio fischeri

Heterogeneous Response to a Quorum-Sensing Signal in the Luminescence of Individual Vibrio fischeri

Novel Reporter for Identification of Interference with Acyl Homoserine Lactone and Autoinducer-2 Quorum Sensing

Dynamics of the quorum sensing switch: stochastic and non-stationary effects

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