A stochastic model of
            <i>Escherichia coli</i>
            AI‐2 quorum signal circuit reveals alternative synthesis pathways

Li, Jun; Wang, Liang; Hashimoto, Yoshifumi; Tsao, Chen Yu; Wood, Thomas K.; Valdés, James J.; Zafiriou, Evanghelos; Bentley, William E.

doi:10.1038/msb4100107

Cited by 54 publications

(53 citation statements)

References 75 publications

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“…However, AI-2 is taken up by Lsr mutants. Also, intracellular AI-2 by deletion of ydgG has been noted (35), and (43). All are consistent with the existence of AI-2 (or its anomers) inside cells.…”

Section: Discussionsupporting

confidence: 66%

Quorum Sensing in Escherichia coli Is Signaled by AI-2/LsrR: Effects on Small RNA and Biofilm Architecture

et al. 2007

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The regulatory network for the uptake of Escherichia coli autoinducer 2 (AI-2) is comprised of a transporter complex, LsrABCD; its repressor, LsrR; and a cognate signal kinase, LsrK. This network is an integral part of the AI-2 quorum-sensing (QS) system. Because LsrR and LsrK directly regulate AI-2 uptake, we hypothesized that they might play a wider role in regulating other QS-related cellular functions. In this study, we characterized physiological changes due to the genomic deletion of lsrR and lsrK. We discovered that many genes were coregulated by lsrK and lsrR but in a distinctly different manner than that for the lsr operon (where LsrR serves as a repressor that is derepressed by the binding of phospho-AI-2 to the LsrR protein). An extended model for AI-2 signaling that is consistent with all current data on AI-2, LuxS, and the LuxS regulon is proposed. Additionally, we found that both the quantity and architecture of biofilms were regulated by this distinct mechanism, as lsrK and lsrR knockouts behaved identically. Similar biofilm architectures probably resulted from the concerted response of a set of genes including flu and wza, the expression of which is influenced by lsrRK. We also found for the first time that the generation of several small RNAs (including DsrA, which was previously linked to QS systems in Vibrio harveyi) was affected by LsrR. Our results suggest that AI-2 is indeed a QS signal in E. coli, especially when it acts through the transcriptional regulator LsrR.Bacteria communicate with each other through small "hormone-like" organic molecules referred to as autoinducers. Autoinducer-based bacterial cell-to-cell communication, enabling population-based multicellularity, has been termed quorum sensing (QS) (27). Cellular functions controlled by QS are varied and reflect the needs of a particular bacterial species for inhabiting a given niche (10,38,65).QS among Escherichia coli and Salmonella strains has been a topic of great interest, and different intercellular signaling systems have been identified: that mediated by the LuxR homolog SdiA; the LuxS/autoinducer 2 (AI-2) system, an AI-3 system, and a signaling system mediated by indole (2,19,36,57,61,68). Among these systems, the LuxS/AI-2 system possesses the unique feature of endowing cell population-dependent behavior while interacting with central metabolism through the intracellular activated methyl cycle (20,21,45,65,73). Therefore, it has the potential to influence both gene regulation and bacterial fitness.AI-2's function has been studied using luxS mutants and by adding either conditioned medium or in vitro-synthesized AI-2 to bacterial cultures. It is noteworthy that the luxS transcription profile is not synchronous with the accumulation profile of extracellular AI-2 in bacterial supernatants (5,31,75). In E.coli, extracellular AI-2 activity peaks during the mid-to lateexponential phase and rapidly decreases during entry into the stationary phase. A corresponding decrease in LuxS protein levels is not observed (31,75). The disap...

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Section: Discussionsupporting

confidence: 66%

Quorum Sensing in Escherichia coli Is Signaled by AI-2/LsrR: Effects on Small RNA and Biofilm Architecture

et al. 2007

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“…They also added molecular noise. Li et al (2006) studied the luxS-derived autoinducer system AI-2 of E. coli employing a stochastic mathematical model often used in quantitative molecular biology called stochastic petri dish (SPN), see Goss and Peccoud (1998). Thanks to their integrative approach they were able to unveil an alternative pathway for AI-2 synthesis.…”

Section: Models Of the Qs Molecular Mechanismmentioning

confidence: 99%

“…swimming, foraging) Tang et al (2007), van Gestel et al (2012) Virulence Pseudomonas aeruginosa Dockery and Keener (2001), Fagerlind et al (2003Fagerlind et al ( , 2005, Viretta and Fussenegger (2004), Netotea et al (2009) AHL, AHQ Koerber et al (2005), Jabbari et al (2010), Gustafsson et al (2004) AIP Escherichia coli Li et al (2006) AI-2, Indole Lee et al (2007) See Taga and Bassler (2003), Miller and Bassler (2001) and West et al (2012) for a more comprehensive list. Note that not all models concentrate on a particular bacterium…”

Section: Hunter Et Al (2013) Ahlmentioning

confidence: 99%

Mathematical Modelling of Bacterial Quorum Sensing: A Review

2016

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Bacterial quorum sensing (QS) refers to the process of cell-to-cell bacterial communication enabled through the production and sensing of the local concentration of small molecules called autoinducers to regulate the production of gene products (e.g. enzymes or virulence factors). Through autoinducers, bacteria interact with individuals of the same species, other bacterial species, and with their host. Among QS-regulated processes mediated through autoinducers are aggregation, biofilm formation, bioluminescence, and sporulation. Autoinducers are therefore "master" regulators of bacterial lifestyles. For over 10 years, mathematical modelling of QS has sought, in parallel to experimental discoveries, to elucidate the mechanisms regulating this process. In this review, we present the progress in mathematical modelling of QS, highlighting the various theoretical approaches that have been used and discussing some of the insights that have emerged. Modelling of QS has benefited almost from the onset of the involvement of experimentalists, with many of the papers which we review, published in non-mathematical journals. This review therefore attempts to give a broad overview of the topic to the mathematical biology community, as well as the current modelling efforts and future challenges.B Judith Pérez-Velázquez

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“…Since LsrR contains a predicted HTH DNA-binding domain, it has been suggested to repress the transcription of the lsr operon and itself by directly binding to their promoters. In order to determine whether LsrR can bind to the lsrA and lsrR promoter regions, we carried out gel evidence showed that in V. harveyi, AI-2 is (2S, 4S)-2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran-borate (S-THMF-borate); and in E. coli and S. typhimurium, AI-2 is (2R, 4S)-2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran (R-THMF) [10,[16][17][18][19][20][21][22].…”

Section: Lsrr Binds To Lsra and Lsrr Promotersmentioning

confidence: 99%

LsrR-binding site recognition and regulatory characteristics in Escherichia coli AI-2 quorum sensing

et al. 2009

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In quorum sensing (QS) process, bacteria regulate gene expression by utilizing small signaling molecules called autoinducers in response to a variety of environmental cues. Autoinducer 2 (AI-2), a QS signaling molecule proposed to be involved in interspecies communication, is produced by many species of gram-negative and gram-positive bacteria. In Escherichia coli and Salmonella typhimurium, the extracellular AI-2 is imported into the cell by a transporter encoded by the lsr operon. Upstream of the lsr operon, there is a divergently transcribed gene encoding LsrR, which was reported previously to repress the transcription of the lsr operon and itself. Here, we have demonstrated for the first time that LsrR represses the transcription of the lsr operon and itself by directly binding to their promoters using gel shift and DNase I footprinting assays. The β-galactosidase reporter assays further suggest that two motifs in both the lsrR and lsrA promoter regions are crucial for the LsrR binding. Furthermore, in agreement with the conclusion that phosphorylated AI-2 can relieve the repression of LsrR in previous studies, our data show that phospho-AI-2 renders LsrR unable to bind to its own promoter in vitro.

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A stochastic model of Escherichia coli AI‐2 quorum signal circuit reveals alternative synthesis pathways

Cited by 54 publications

References 75 publications

Quorum Sensing in Escherichia coli Is Signaled by AI-2/LsrR: Effects on Small RNA and Biofilm Architecture

Quorum Sensing in Escherichia coli Is Signaled by AI-2/LsrR: Effects on Small RNA and Biofilm Architecture

Mathematical Modelling of Bacterial Quorum Sensing: A Review

LsrR-binding site recognition and regulatory characteristics in Escherichia coli AI-2 quorum sensing

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