1887

Abstract

Many bacteria produce extracellular molecules which function in cell-to-cell communication. One of these molecules, autoinducer 2 (AI-2), was first described as an extracellular signal produced by to control luciferase expression. Subsequently, a number of bacteria have been shown to possess AI-2 activity in their culture supernatants, and bear the gene product, which is required for AI-2 synthesis. In , and , encoding a 5′-methylthioadenosine/-adenosylhomocysteine nucleosidase (MTA/SAH’ase), form an operon, suggesting that -adenosylhomocysteine (SAH) or 5′-methylthioadenosine (MTA) serves as a substrate for AI-2 production. Cell-free extracts of MG1655, but not DH5α (which carries a frame-shift mutation) were capable of generating AI-2 activity upon addition of SAH, but not MTA. -Ribosyl-homocysteine (RH) derived from SAH also served as a substrate in MG1655 extracts. RH-supplemented cell-free extracts of , a bacterium that lacks , only generated AI-2 activity following the introduction of a plasmid containing the operon. In addition, defined systems consisting of the purified LuxS proteins from , , or converted RH to homocysteine and a compound that exhibits AI-2 activity.4-Hydroxy-5-methyl-3()-furanone was identified by mass spectrometry analysis as a major product formed in this reaction. In MG1655, expression of T3SH [the bacteriophage T3 -adenosylmethionine (SAM) hydrolase] significantly reduced AI-2 activity in culture supernatants, suggesting that AI-2 production is limited by the amount of SAH produced in SAM-dependent transmethylase reactions. The authors suggest that the LuxS protein has an important metabolic function in the recycling of SAH. They also show that is capable of removing AI-2 activity, implying that this molecule may act as a nutrient. In many bacteria AI-2 may in fact represent not a signal molecule but a metabolite which is released early and metabolized in the later stages of growth.

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2002-04-01
2021-07-28
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References

  1. Bassler B. L. 1999; How bacteria talk to each other: regulation of gene expression by quorum sensing. Curr Opin Microbiol 2:582–587 [CrossRef]
    [Google Scholar]
  2. Bassler B. L., Wright M., Silverman M. R. 1994; Multiple signalling systems controlling expression of luminescence in Vibrio harveyi : sequence and function of genes encoding a second sensory pathway. Mol Microbiol 13:273–286 [CrossRef]
    [Google Scholar]
  3. Bassler B. L., Greenberg E. P., Stevens A. M. 1997; Cross-species induction of luminescence in the quorum sensing bacterium Vibrio harveyi . J Bacteriol 179:4043–4045
    [Google Scholar]
  4. Blank I., Fay L. B. 1996; Formation of 4-hydroxy-2,5-dimethyl-3( 2H )-furanone and 4-hydroxy-2(or 5)-5(or 2) methyl-3( 2H )-furanone through Maillard reaction based on pentose sugars. J Agric Food Chem 44:531–536 [CrossRef]
    [Google Scholar]
  5. Burgess N., Kirke D., Williams P., Winzer K., Hardie K. R., Meyers N. L., Aduse-Opoku J., Curtis M. A., Cámara M. 2002; LuxS-dependent quorum sensing in Porphyromonas gingivalis modulates protease and haemagglutinin activities but is not essential for virulence. Microbiology 148:763–772
    [Google Scholar]
  6. Chung W. O., Park Y., Lamont R. J., McNab R., Barbieri B., Demuth D. R. 2001; Signaling system in Porphyromonas gingivalis based on a LuxS protein. J Bacteriol 183:3903–3909 [CrossRef]
    [Google Scholar]
  7. Cornell K. A., Riscoe M. K. 1998; Cloning and expression of Escherichia coli 5′-methylthioadenosine/ S -adenosylhomocysteine nucleosidase: identification of the pfs gene product. Biochim Biophys Acta 13968–14 [CrossRef]
    [Google Scholar]
  8. Day W. A., Maurelli A. T. 2001; Shigella flexneri LuxS quorum sensing system modulates virB expression but is not essential for virulence. Infect Immun 69:15–23 [CrossRef]
    [Google Scholar]
  9. DeLisa M. P., Valdes J. J., Bentley W. E. 2001a; Mapping stress-induced changes in autoinducer AI-2 production in chemostat-cultivated Escherichia coli K-12. J Bacteriol 183:2918–2928 [CrossRef]
    [Google Scholar]
  10. DeLisa M. P., Wu C. F., Wang L., Valdes J. J., Bentley W. E. 2001b; DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli . J Bacteriol 183:5239–5247 [CrossRef]
    [Google Scholar]
  11. Dong Y. H., Xu J. L., Li X. Z., Zhang L. H. 2000; AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora . Proc Natl Acad Sci USA 97:3526–3531 [CrossRef]
    [Google Scholar]
  12. Duerre J. A. 1962; A hydrolytic nucleosidase acting on S -adenosylhomocysteine and on 5′-methylthioadenosine. J Biol Chem 237:3737–3741
    [Google Scholar]
  13. Duerre J. A., Miller C. H. 1966; Cleavage of S -ribosyl-l-homocysteine by extracts from Escherichia coli . J Bacteriol 91:1210–1217
    [Google Scholar]
  14. Duerre J. A., Baker D. J., Salisbury L. 1971; Structure elucidation of a carbohydrate derived from S -ribosylhomocysteine by enzymatic cleavage. Fed Proc 30:88
    [Google Scholar]
  15. Farine J.-P., Le Quere J.-L., Duffy J., Semon E., Brossut R. 1993; 4-Hydroxy-5-methyl-3( 2H) -furanone and 4-hydroxy-2,5-dimethyl-3( 2H) -furanone, two components of the male sex pheromone of Eurycotis flordana (Walker) (Insecta, Blattidae, Polyzosteriinae). Biosci Biotechnol Biochem 57:2026–2030 [CrossRef]
    [Google Scholar]
  16. Forsyth M. H., Cover T. L. 2000; Intercellular communication in Helicobacter pylori : luxS is essential for the production of an extracellular signaling molecule. Infect Immun 68:3193–3199 [CrossRef]
    [Google Scholar]
  17. Gardiner S. M., Chhabra S. R., Harty C., Williams P., Pritchard D. I., Bycroft B. W., Bennett T. 2001; Haemodynamic effects of the bacterial quorum sensing signal molecule, N -(3-oxododecanoyl)-l-homoserine lactone, in conscious, normal and endotoxaemic rats. Br J Pharmacol 133:1047–1054 [CrossRef]
    [Google Scholar]
  18. Gordon R. K., Miura G. A., Alonso T., Chiang P. K. 1987; S -Adenosylmethionine and its sulfur metabolites. Methods Enzymol 143:191–195
    [Google Scholar]
  19. Greenberg E. P. 1999; Quorum sensing in Gram-negative bacteria: acylhomoserine lactone signalling and cell–cell communication. In Microbial Signalling and CommunicationSociety for General Microbiology Symposium no. 57 pp 71–84 Edited by England R., Hobbs G., Bainton N., Roberts D. McL. Cambridge: Cambridge University Press;
    [Google Scholar]
  20. Greenberg E. P., Hastings J. W., Ulitzer S. 1979; Induction of luciferase sunthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120:87–91 [CrossRef]
    [Google Scholar]
  21. Greene R. C. others 1996; Biosynthesis of methionine. In Escherichia coli and Salmonella: Cellular and Molecular Biology . , 2nd edn. vol 1 pp 542–560 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
  22. Guzman L.-M., Belin D., Carson M. J., Beckwith J. 1995; Tight regulation, modulation, and high level expression by vectors containing the arabinose pBAD promoter. J Bacteriol 177:4121–4130
    [Google Scholar]
  23. Hayashida Y., Hatano M., Tamura Y., Kakimoto M., Nishimura K., Igoshi K., Kobayashi H., Kuriyama H. 2001; 4-Hydroxy-2,5-dimethyl-3( 2H )-furanone (HDMF) production in simple media by lactic acid bacterium, Lactococcus lactis subsp. cremoris IFO 3427. J Biosci Bioeng 91:97–99 [CrossRef]
    [Google Scholar]
  24. Hiramoto K., Sekiguchi K., Ayuha K., Aso-o R., Morya N., Kato T., Kikugawa K. 1996; DNA breaking activity and mutagenicity of soy sauce: characterization of the active components and identification of 4-hydroxy-5-methyl-3( 2H )-furanone. Mutat Res 359:119–132 [CrossRef]
    [Google Scholar]
  25. Jiang Y., Camara M., Chhabra S. R., Hardie K. R., Bycroft B. W., Lazdunski A., Salmond G. P., Stewart G. S., Williams P. 1998; In vitro biosynthesis of the Pseudomonas aeruginosa quorum-sensing signal molecule N -butanoyl-l-homoserine lactone. Mol Microbiol 28:193–203
    [Google Scholar]
  26. Joyce E. A., Bassler B. L., Wright A. 2000; Evidence for a signalling system in Helicobacter pylori : detection of a luxS -encoded autoinducer. J Bacteriol 182:3638–3643 [CrossRef]
    [Google Scholar]
  27. Kleerebezem M., Quadri L. E. N., Kuipers O. P., de Vos W. M. 1997; Quorum sensing by peptide pheromones and two component signal transduction systems in Gram-positive bacteria. Mol Microbiol 24:895–904 [CrossRef]
    [Google Scholar]
  28. Lazazzera B. A., Grossman A. D. 1998; The ins and outs of peptide signalling. Trends Microbiol 6:288–294 [CrossRef]
    [Google Scholar]
  29. Leadbetter J. R., Greenberg E. P. 2000; Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax paradoxus . J Bacteriol 182:6921–6926 [CrossRef]
    [Google Scholar]
  30. Lyon W. R., Madden J. C., Levin J. C., Stein J. L., Caparon M. G. 2001; Mutation of luxS affects growth and virulence factor expression in Streptococcus pyogenes . Mol Microbiol 42:145–157
    [Google Scholar]
  31. Miller C. H., Duerre J. A. 1968; S -Ribosylhomocysteine cleavage enzyme from Escherichia coli . J Biol Chem 243:92–97
    [Google Scholar]
  32. Moré M. I., Finger L. D., Stryker J. L., Fuqua C., Eberhard A., Winans S. C. 1996; Enzymatic synthesis of a quorum-sensing autoinducer through the use of defined substrates. Science 272:1655–1658 [CrossRef]
    [Google Scholar]
  33. Nedvidek W., Ledl F., Fischer P. 1992; Detection of 5-hydroxymethyl-2-methyl-3( 2H )-furanone and of α-dicarbonyl compounds in reaction mixtures of hexoses and pentoses with different amines. Z Lebensm-Unters-Forsch 194:222–228 [CrossRef]
    [Google Scholar]
  34. Newman E. B., Budman L. I., Chan E. C., Greene R. C., Lin R. T., Woldringh C. L., D’Ari R. 1998; Lack of S -adenosylmethionine results in a cell divison defect in Escherichia coli . J Bacteriol 180:3614–3619
    [Google Scholar]
  35. Novick R. P. 1999; Regulation of pathogenicity in Staphylococcus aureus by a peptide-based density-sensing system In Cell–Cell Signaling in Bacteria . pp 129–146 Edited by Dunny G. M., Winans S. C. Washington, DC: American Society for Microbiology;
  36. Novick R. P., Muir W. M. 1999; Virulence gene regulation by peptides in staphylococci and other Gram-positive bacteria. Cur Opin Microbiol 2:40–45 [CrossRef]
    [Google Scholar]
  37. Posnick L. M., Samson L. D. 1999; Influence of S -adenosylmethionine pool size on spontaneous mutation, dam methylation, and cell growth. J Bacteriol 181:6756–6762
    [Google Scholar]
  38. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  39. Schauder S., Shokat K., Surette M. G., Bassler B. L. 2001; The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum sensing signal molecule. Mol Microbiol 41:463–476 [CrossRef]
    [Google Scholar]
  40. Schweizer H. P. 1991; Escherichia–Pseudomonas shuttle vectors derived from pUC18/19. Gene 97:109–121 [CrossRef]
    [Google Scholar]
  41. Shimizu S., Shiozaki S., Ohshiro T., Yamada H. 1984; Occurrence of S -adenosylhomocysteine in prokaryote cells. Characterization of the enzyme from Alcaligenes faecalis and role of the enzyme in the activated methyl cycle. Eur J Biochem 141:385–392 [CrossRef]
    [Google Scholar]
  42. Slaughter J. C. 1999; The naturally occuring furanones: formation and function from pheromone to food. Biol Rev Camb Philos Soc 74:259–276 [CrossRef]
    [Google Scholar]
  43. Smith A. W., Iglewski B. H. 1989; Transformation of Pseudomonas aeruginosa by electroporation. Nucleic Acids Res 17:105–109
    [Google Scholar]
  44. Sperandio V., Mellies J. L., Nguyen W., Shin S., Kaper J. B. 1999; Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli . Proc Natl Acad Sci USA 96:15196–15201 [CrossRef]
    [Google Scholar]
  45. Sperandio V., Torres A. G., Giron J. A., Kaper J. B. 2001; Quorum sensing is a global regulatory mechanism in enterohemorrhagic Escherichia coli O157: H7. J Bacteriol 183:5187–5197 [CrossRef]
    [Google Scholar]
  46. Surette M. G., Bassler B. L. 1998; Quorum sensing in Escherichia coli and Salmonella typhimurium . Proc Natl Acad Sci USA 95:7046–7050 [CrossRef]
    [Google Scholar]
  47. Surette M. G., Bassler B. L. 1999; Regulation of autoinducer production in Salmonella typhimurium . Mol Microbiol 31:585–595 [CrossRef]
    [Google Scholar]
  48. Surette M. G., Miller M. B., Bassler B. L. 1999; Quorum sensing in Escherichia coli , Salmonella typhimurium , and Vibrio harveyi : a new family of genes responsible for autoinducer production. Proc Natl Acad Sci U S A 96:1639–1644 [CrossRef]
    [Google Scholar]
  49. Telford G., Wheeler D., Williams P., Tomkins P. T., Appleby P., Sewell H., Stewart G. S. A. B., Bycroft B. W., Pritchard D. I. 1998; The Pseudomonas aeruginosa quorum sensing signal molecule, N- (3-oxododecanoyl)-l-homoserine lactone, has immunomodulatory activity. Infect Immun 66:36–42
    [Google Scholar]
  50. Walker R. D., Duerre J. A. 1975; S -Adenosylmethionine metabolism in various species. Can J Biochem 53:312–319 [CrossRef]
    [Google Scholar]
  51. Whitfield F. B., Mottram D. S. 1999; Investigation of the reaction between 4-hydroxy-5-methyl-3( 2H )-furanone and cysteine or hydrogen sulfide at pH 4·5. J Agric Food Chem 47:1626–1634 [CrossRef]
    [Google Scholar]
  52. Whitfield F. B., Mottram D. S. 2001; Heterocyclic volatiles formed by heating cysteine or hydrogen sulfide with 4-hydroxy-5-methyl-3( 2H )-furanone at pH 6·5. J Agric Food Chem 49:816–822 [CrossRef]
    [Google Scholar]
  53. Williams P., Camara M., Hardman A. & 7 other authors; 2000; Quorum sensing and the population dependent control of virulence. Philos Trans R Soc Lond B Biol Sci 355:667–680 [CrossRef]
    [Google Scholar]
  54. Winzer K., Sun Y.-H., Green A., Delory M., Blackley D., Hardie K. R., Baldwin T. J., Tang C. 2002; The role of Neisseria meningitidis luxS in cell-to-cell signaling and bacteraemia. Infect Immun in press
    [Google Scholar]
  55. Withers H., Swift S., Williams P. 2001; Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr Opin Microbiol 4:186–193 [CrossRef]
    [Google Scholar]
  56. Yamashita N., Murata M., Inoue S., Hiraki Y., Yoshiaga T., Kawanishi S. 1998; Superoxide formation and DNA damage induced by a fragrant furanone in the presence of copper (II). Mutat Res 397:191–201 [CrossRef]
    [Google Scholar]
  57. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119 [CrossRef]
    [Google Scholar]
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