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.

Download full-text


Available from: Julia Semmelhack, Jul 03, 2015
1 Follower
  • Source
    [Show abstract] [Hide abstract]
    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.
  • Source
    [Show abstract] [Hide abstract]
    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.
    FEMS Microbiology Letters 09/2013; 350(1). DOI:10.1111/1574-6968.12275 · 2.72 Impact Factor
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Small molecule probes have been used extensively to explore biologic systems and elucidate cellular signaling pathways. In this study, we use an inhibitor of bacterial communication to monitor changes in the proteome of Salmonella enterica serovar Typhimurium with the aim of discovering unrecognized processes regulated by AI-2-based quorum-sensing (QS), a mechanism of bacterial intercellular communication that allows for the coordination of gene expression in a cell density-dependent manner. In S. typhimurium, this system regulates the uptake and catabolism of intercellular signals and has been implicated in pathogenesis, including the invasion of host epithelial cells. We demonstrate that our QS antagonist is capable of selectively inhibiting the expression of known QS-regulated proteins in S. typhimurium, thus attesting that QS inhibitors may be used to confirm proposed and elucidate previously unidentified QS pathways without relying on genetic manipulation.
    Chemistry & biology 07/2013; 20(7):903-11. DOI:10.1016/j.chembiol.2013.05.009 · 6.59 Impact Factor