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The LuxS-dependent autoinducer AI-2 controls the expression of an ABC transporter that functions in AI-2 uptake in Salmonella typhimurium

Department of Molecular Biology, Princeton University, Princeton, NJ 08544-1014, USA.
Molecular Microbiology (Impact Factor: 5.03). 12/2001; 42(3):777-93.
Source: PubMed

ABSTRACT In a process called quorum sensing, bacteria communicate with one another using secreted chemical signalling molecules termed autoinducers. A novel autoinducer called AI-2, originally discovered in the quorum-sensing bacterium Vibrio harveyi, is made by many species of Gram-negative and Gram-positive bacteria. In every case, production of AI-2 is dependent on the LuxS autoinducer synthase. The genes regulated by AI-2 in most of these luxS-containing species of bacteria are not known. Here, we describe the identification and characterization of AI-2-regulated genes in Salmonella typhimurium. We find that LuxS and AI-2 regulate the expression of a previously unidentified operon encoding an ATP binding cassette (ABC)-type transporter. We have named this operon the lsr (luxS regulated) operon. The Lsr transporter has homology to the ribose transporter of Escherichia coli and S. typhimurium. A gene encoding a DNA-binding protein that is located adjacent to the Lsr transporter structural operon is required to link AI-2 detection to operon expression. This gene, which we have named lsrR, encodes a protein that represses lsr operon expression in the absence of AI-2. Mutations in the lsr operon render S. typhimurium unable to eliminate AI-2 from the extracellular environment, suggesting that the role of the Lsr apparatus is to transport AI-2 into the cells. It is intriguing that an operon regulated by AI-2 encodes functions resembling the ribose transporter, given recent findings that AI-2 is derived from the ribosyl moiety of S-ribosylhomocysteine.

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    • "S-Ribosylhomocysteine lyase is encoded by luxS gene and is involved in the synthesis of autoinducer 2 (Al-2), which is secreted by bacteria during quorum sensing [64, 65]. Changes in the cell density during the transition of growth phases are likely to stimulate the expression of S-ribosylhomocysteine lyase and the subsequent synthesis of Al-2 in L. lactis M4. "
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    ABSTRACT: Lactococcus lactis is the most studied mesophilic fermentative lactic acid bacterium. It is used extensively in the food industry and plays a pivotal role as a cell factory and also as vaccine delivery platforms. The proteome of the Malaysian isolated L. lactis M4 dairy strain, obtained from the milk of locally bred cows, was studied to elucidate the physiological changes occurring between the growth phases of this bacterium. In this study, ultraperformance liquid chromatography nanoflow electrospray ionization tandem mass spectrometry (UPLC- nano-ESI-MS(E)) approach was used for qualitative proteomic analysis. A total of 100 and 121 proteins were identified from the midexponential and early stationary growth phases, respectively, of the L. lactis strain M4. During the exponential phase, the most important reaction was the generation of sufficient energy, whereas, in the early stationary phase, the metabolic energy pathways decreased and the biosynthesis of proteins became more important. Thus, the metabolism of the cells shifted from energy production in the exponential phase to the synthesis of macromolecules in the stationary phase. The resultant proteomes are essential in providing an improved view of the cellular machinery of L. lactis during the transition of growth phases and hence provide insight into various biotechnological applications.
    03/2014; 2014(12):642891. DOI:10.1155/2014/642891
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    • "After binding, the Lsr ABC transporter that consists of LsrC and LsrA transports AI-2 into the cell where it is phosphorylated by LsrK. AI-2 in its phosphorylated form interacts with the LsrR that is a transcriptional repressor, in order to alleviate repression of the operon lsr which may up regulate other operons (Taga et al., 2001). In Gram-negative and Gram-positive bacteria a wide range of LuxS/AI-2 systems have been found which has proposed the idea that the AI-2 system is utilized for cross-species signaling process by organisms that live in mixed-species communities like biofilms (Xavier and Bassler, 2003). "
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    ABSTRACT: The chemical signal molecules called autoinducers are produced and released by the quorum sensing bacteria to levels dominating the increasing cell-population density. The attainment of minimal threshold stimulatory concentration of an autoinducer leads to an alteration in gene expression. Both Gram-positive and Gram-negative bacteria are capable of using quorum sensing communication circuits for regulating a diverse array of physiological activities. These activities include symbiosis, competence, virulence, conjugation, antibiotic production, sporulation, motility and biofilm formation. The Gram-negative bacteria use acylated homoserine lactones as autoinducers, while Gram-positive bacteria use processed oligo-peptides to communicate. In the field of quorum sensing revealed, cell to cell communication via autoinducers both within and between bacterial species. The establishment of enormous data in this field suggests autoinducers acquiring specific responses from host organisms. Despite the difference in chemical signals, signal relay mechanisms and the target genes controlled by the bacterial quorum sensing systems, the ability to communicate with one another allows bacteria to coordinate the gene expression as well as the behaviour of the entire community. This process presumably confers upon the bacteria some of the qualities of higher organisms. The evolution of quorum sensing systems in bacteria thus could have been one of the early steps in the development of multicellularity.
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    • "Synthesis of AI-2 depends on luxS, which is the product of S-ribosylhomocysteine lyase. luxS was first identified in Vibrio harveyi, Escherichia coli, and Salmonella typhimurium, and its expression has been associated with virulence in E. coli and Streptococcus pyogenes (DeLisa et al., 2001; Lyon et al., 2001) and biofilm formation in Bacillus cereus (Taga et al., 2001; Xavier & Bassler, 2005a, b; Auger et al., 2006). More than 40 bacterial species harbor luxS, and this apparent universality makes it attractive for evolutionary analyses (Bassler, 1999; Surette et al., 1999; Winzer et al., 2003; Rezzonico & Duffy, 2008). "
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    ABSTRACT: Interspecies bacterial communication is mediated by autoinducer-2, whose synthesis depends on luxS. Due to the apparent universality of luxS (present in more than 40 bacterial species), it may have an ancient origin; however, no direct evidence is currently available. We amplified luxS in bacteria isolated from 25- to 40-million-year-old amber. The phylogenies and molecular clocks of luxS and the 16S rRNA gene from ancient and extant bacteria were determined as well. Luminescence assays using Vibrio harveyi BB170 aimed to determine the activity of luxS. While the phylogeny of luxS was very similar to that of extant Bacillus spp., amber isolates exhibited unique 16S rRNA gene phylogenies. This suggests that luxS may have been acquired by horizontal transfer millions of years ago. Molecular clocks of luxS suggest slow evolutionary rates, similar to those of the 16S rRNA gene and consistent with a conserved gene. Dendograms of the 16S rRNA gene and luxS show two separate clusters for the extant and ancient bacteria, confirming the uniqueness of the latter group.
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