LuxS quorum sensing: More than just a numbers game

Current Opinion in Microbiology

Volumn 6, Issue 2, 2003, Pages 191-197

  Xavier, Karina B ^a   Bassler, Bonnie L ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ACETYLACETONE; ADENINE; ADENOSINE DERIVATIVE; BORON; HOMOCYSTEINE; LACTONE; OLIGOPEPTIDE; PROTEIN; RIBOSE; SYNTHETASE;

BACTERIUM; CELL COMMUNICATION; GENE EXPRESSION; NONHUMAN; REVIEW;

BACTERIA (MICROORGANISMS);

EID: 0037676088     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1369-5274(03)00028-6     Document Type: Review

References (35)

1. Miller MB, Bassler BL: Quorum sensing in bacteria. Annu Rev Microbiol 2001, 55:165-199.
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3. Miller MB, Skorupski K, Lenz DH, Taylor RK, Bassler BL: Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 2002, 110:303-314. Using the Vibrio harveyi luciferase operon (luxCDABE) as a heterologous reporter of quorum-sensing-controlled gene expression, the authors show that three parallel quorum-sensing circuits exist in V. cholerae. A series of single, double and triple mutants were constructed, and an analysis of their phenotypes used to define the signaling circuitry. Mouse infection, toxin and pilus assays were used to demonstrate that the three quorum-sensing systems jointly regulate virulence.
4. Derzelle S, Duchaud E, Kunst F, Danchin A, Bertin P: Identification, characterization, and regulation of a cluster of genes involved in carbapenem biosynthesis in Photorhabdus luminescens. Appl Environ Microbiol 2002, 68:3780-3789. Photorhabdus luminescens lives in symbiotic association with a soil nematode. The nematode expels the bacteria into susceptible insects, the bacteria kill the insects, and this action provides nutrients for the nematode to use to grow and reproduce. The bacteria also release a battery of antibiotics that keep the insect carcass free of other microorganisms. A luxS-null P. luminescens mutant shows altered timing of expression of cpmA, a gene required for biosynthesis of the antibiotic carbapenem. Correct timing of carbapenem production is important for ensuring nematode reproduction in the dead insect.
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8. Schauder S, Shokat K, Surette MG, Bassler BL: The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 2001, 41:463-476. Genomic sequence gazing was used to show that luxS exists in an operon with two genes involved in S-adenosylmethionine (SAM) metabolism (metK and pfs) in B. burgdorferi. This finding inspired the idea that LuxS, in all bacteria, might act in a pathway with MetK and Pfs. This work shows this is indeed the case, and it contains a detailed analysis of the three-step route for Al-2 biosynthesis. Purified proteins are used to produce Al-2 activity in vitro.
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11. Winzer K, Hardie KR, Burgess N, Doherty N, Kirke D, Holden MT, Linforth R, Cornell KA, Taylor AJ, Hill PJ et al.: LuxS: its role in central metabolism and the in vitro synthesis of 4-hydroxy 5-methyl 3(2H)-furanone. Microbiology 2002, 148:909-922.
12. Bassler BL, Wright M, Showalter RE, Silverman MR: Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence. Mol Microbiol 1993, 9:773-786.
13. Bassler BL, Wright M, Silverman MR: Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol 1994, 13:273-286.
14. Ohtani K, Hayashi H, Shimizu T: The luxS gene is involved in cell-cell signalling for toxin production in Clostridium perfringens. Mol Microbiol 2002, 44:171-179. The pathogen Clostridium perfringens produces Al-2 activity that peaks in mid-late exponential growth phase and rapidly disappears upon entrance into stationary phase. A C. perfringens luxS mutant produces lower alpha-, kappa-, and theta toxin compared with wild-type C. perfringens. This work shows that the luxS system controls toxin production by transcriptional and post-transcriptional regulatory mechanisms. Al-2 in cell-free culture activated transcription of the theta toxin gene (pfoA) in a luxS mutant. The authors suggest that one role of luxS is to regulate the timing of toxin production.
15. Stevenson B, Babb K: LuxS-mediated quorum sensing in Borrelia burgdorferi, the lyme disease spirochete. Infect Immun 2002, 70:4099-4105. Borrelia burgdorferi displays altered production of many proteins (as assayed by two-dimensional gels) in response to Al-2 produced by an Escherichia coli luxS mutant carrying the B. burgdorferi luxS gene. These proteins include complement-regulating factors called H-binding Erp proteins (Erp A, -I and -N). Production of Al-2 by B. burgdorferi was not observed, suggesting that either Al-2 of B. burgdorferi cannot be detected by the V. harveyi Al-2 reporter strain, or Al-2 is not produced under in vitro conditions. The authors speculate that the spirochete uses Al-2 quorum sensing in the tick host.
16. Surette MG, Bassler BL: Regulation of autoinducer production in Salmonella typhimurium. Mol Microbiol 1999, 31:585-595.
17. DeLisa MP, Valdes JJ, Bentley WE: Mapping stress-induced changes in autoinducer Al-2 production in chemostatcultivated Escherichia coli K-12. J Bacteriol 2001, 183:2918-2928. The timing and level of Al-2 production was investigated in Escherichia coli W3110 chemostat cultures. Al-2 activity increased following addition of glucose, Fe (III), NaCl, and dithiothreitol, and decreased under aerobiosis and amino acid starvation.
18. Beeston AL, Surette MG: pfs-dependent regulation of autoinducer 2 production in Salmonella enterica serovar typhimurium. J Bacteriol 2002, 184:3450-3456.
19. - random lacZ reporter insertions was generated and screened for Al-2 regulated fusions. This experiment reveals a previously uncharacterized ABC transporter, which is shown by several criteria to be responsible for transporting extracellular Al-2 into the cells. This work identifies the mechanism responsible for Al-2 disappearance from stationary-phase culture fluids, which is observed in many Al-2-producing bacteria.
20. Fong KP, Chung WO, Lamont RJ, Demuth DR: Intra- and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infect Immun 2001, 69:7625-7634. Many periodontal pathogens including Actobacillus actinomycetemcomitans have LuxS and produce Al-2. Al-2 in conditioned medium, prepared from an Escherichia coli luxS mutant expressing the A. actinomycetemcomitans luxS gene promotes production of leukotoxin, as judged by protein levels and activity assays. The leukotoxin induces apoptosis in host cells. RT-PCR is used to show that Al-2 also induces expression of afuA, a periplasmic iron-transport protein. The conditioned medium from E. coli carrying the A. actinomycetemcomitans luxS gene regulates the expression of uvrB and hasF in Porphyromonas gingivalis.
21. Elvers KT, Park SF: Quorum sensing in Campylobacter jejuni: detection of a luxS encoded signalling molecule. Microbiology 2002, 148:1475-1481.
22. DeLisa MP, Wu CF, Wang L, Valdes JJ, Bentley WE: DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J Bacteriol 2001, 183:5239-5247. DNA microarrays are used to identify genes controlled by Al-2. Global changes in mRNA levels in response to the presence or absence of Al-2 are determined using a luxS mutant strain of Escherichia coli W3110. 242 genes (5.6% of the E. coli genome) were identified that exhibited altered transcription in response to a 300-fold Al-2 differential. These genes include those involved in cell division, DNA processing and cell shape and morphology.
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24. Sperandio V, Torres AG, Kaper JB: Quorum sensing Escherichia coli regulators B and C (QseBC): a novel two-component regulatory system involved in the regulation of flagella and motility by quorum sensing in E. coli. Mol Microbiol 2002, 43:809-821.
25. Sperandio V, Li CC, Kaper JB: Quorum-sensing Escherichia coli regulator A: a regulator of the LysR family involved in the regulation of the locus of enterocyte effacement pathogenicity island in enterohemorrhagic E. coli. Infect Immun 2002, 70:3085-3093.
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27. Winzer K, Sun YH, Green A, Delory M, Blackley D, Hardie KR, Baldwin TJ, Tang CM: Role of Neisseria meningitidis luxS in cell-to-cell signaling and bacteremic infection. Infect Immun 2002, 70:2245-2248.
28. Chung WO, Park Y, Lamont RJ, McNab R, Barbieri B, Demuth DR: Signaling system in Porphyromonas gingivalis based on a LuxS protein. J Bacteriol 2001, 183:3903-3909.
29. Burgess NA, Kirke DF, Williams P, Winzer K, Hardie KR, Meyers NL, Aduse-Opoku J, Curtis MA, Camara M: LuxS-dependent quorum sensing in Porphyromonas gingivalis modulates protease and haemagglutinin activities but is not essential for virulence. Microbiology 2002, 148:763-772.
30. Prouty AM, Schwesinger WH, Gunn JS: Biofilm formation and interaction with the surfaces of gallstones by Salmonella spp. Infect Immun 2002, 70:2640-2649.
31. Day WA Jr, Maurelli AT: Shigella flexneri LuxS quorum-sensing system modulates virB expression but is not essential for virulence. Infect Immun 2001, 69:15-23.
32. Lyon WR, Madden JC, Levin JC, Stein JL, Caparon MG: Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes. Mol Microbiol 2001, 42:145-157. A luxS mutant of Streptococcus pyogenes displays an altered pattern of virulence factor production. Phenotypes include increased transcription of sagA, leading to enhanced haemolytic activity and an altered timing/reduced production of a secreted protease SpeB. The defect in protease activity is caused by the inability of the luxS mutant to secrete and process the precursor polypeptide.
33. Zhu J, Miller MB, Vance RE, Dziejman M, Bassler BL, Mekalanos JJ: Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci USA 2002, 99:3129-3134. Microarrays are used to compare transcriptional expression profiles of the Vibrio cholerae wild-type With a luxO-null mutant. The results indicate that quorum sensing controls the entire virulence cascade by impacting the tcpPH sensory system. Transcriptional reporter fusions and bioassays specifically show that Cholera toxin and the Tcp pilus are not produced in a luxO mutant. Mouse infection assays demonstrate that the quorum-sensing mutant is avirulent.
34. Lilley BN, Bassler BL: Regulation of quorum sensing in Vibrio harveyi by LuxO and sigma-54. Mol Microbiol 2000, 36:940-954.
35. McNab R, Ford SK, El-Sabaeny A, Barbieri B, Cook GS, Lamont RJ: LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 2003, 185:274-278. luxS mutants of S. gordonii and P, gingivalis are shown to be incapable of forming mixed-species biofilms, and restoration of luxS (and Al-2 production) in either strain reverses the defect. This result shows that Al-2-mediated inter-species communication is a required step in mixedspecies biofilm formation and may have implications for the treatment of dental disease. This work also shows that Al-2 controls expression of many carbohydrate metabolism genes in S. gordonii. Presumably the ability of S. gordonii to recognize, adhere to and metabolize carbohydrates is also critical in the formation of dental biofilms.