In Vivo Evidence that S -Adenosylmethionine and Fatty Acid Synthesis Intermediates Are the Substrates for the LuxI Family of Autoinducer Synthases
10.1128/jb.180.10.2644-2651.1998
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACT Many gram-negative bacteria synthesize N -acyl homoserine lactone autoinducer molecules as quorum-sensing signals which act as cell density-dependent regulators of gene expression. We have investigated the in vivo source of the acyl chain and homoserine lactone components of the autoinducer synthesized by the LuxI homolog, TraI. In Escherichia coli , synthesis of N -(3-oxooctanoyl)homoserine lactone by TraI was unaffected in a fadD mutant blocked in β-oxidative fatty acid degradation. Also, conditions known to induce the fad regulon did not increase autoinducer synthesis. In contrast, cerulenin and diazoborine, specific inhibitors of fatty acid synthesis, both blocked autoinducer synthesis even in a strain dependent on β-oxidative fatty acid degradation for growth. These data provide the first in vivo evidence that the acyl chains in autoinducers synthesized by LuxI-family synthases are derived from acyl-acyl carrier protein substrates rather than acyl coenzyme A substrates. Also, we show that decreased levels of intracellular S -adenosylmethionine caused by expression of bacteriophage T3 S -adenosylmethionine hydrolase result in a marked reduction in autoinducer synthesis, thus providing direct in vivo evidence that the homoserine lactone ring of LuxI-family autoinducers is derived from S -adenosylmethionine.

Bibliography

Val, D. L., & Cronan, J. E. (1998). In Vivo Evidence that S -Adenosylmethionine and Fatty Acid Synthesis Intermediates Are the Substrates for the LuxI Family of Autoinducer Synthases. Journal of Bacteriology, 180(10), 2644–2651.

Authors 2
  1. Dale L. Val (first)
  2. John E. Cronan (additional)
References 63 Referenced 106
  1. Alberts A. W. Bell R. M. Vagelos P. R. Acyl carrier protein. XV. Studies of β-ketoacyl-acyl carrier protein synthetase.J. Biol. Chem.247197231903198 / J. Biol. Chem. / Acyl carrier protein. XV. Studies of β-ketoacyl-acyl carrier protein synthetase by Alberts A. W. (1972)
  2. 10.1128/mr.46.3.281-295.1982
  3. Baker H. Frank O. DeAngelis B. Baker E. Branched-chain amino acids overcome cycloleucine growth inhibition in B12 and non-B12-requiring microorganisms.Int. J. Vitam. Nutr. Res.611991319324 / Int. J. Vitam. Nutr. Res. / Branched-chain amino acids overcome cycloleucine growth inhibition in B12 and non-B12-requiring microorganisms by Baker H. (1991)
  4. 10.1111/j.1365-2958.1993.tb01737.x
  5. Beck von Bodman S. Hayman G. T. Farrand S. K. Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor.Proc. Natl. Acad. Sci. USA891992643647 (10.1073/pnas.89.2.643) / Proc. Natl. Acad. Sci. USA / Opine catabolism and conjugal transfer of the nopaline Ti plasmid pTiC58 are coordinately regulated by a single repressor by Beck von Bodman S. (1992)
  6. 10.1128/jb.177.17.5000-5008.1995
  7. 10.1016/S0021-9258(17)37485-9
  8. Black P. N. DiRusso C. C. Molecular and biochemical analysis of fatty acid transport, metabolism, and gene regulation in Escherichia coli.Biochim. Biophys. Acta12101994123145 (10.1016/0005-2760(94)90113-9) / Biochim. Biophys. Acta / Molecular and biochemical analysis of fatty acid transport, metabolism, and gene regulation in Escherichia coli by Black P. N. (1994)
  9. 10.1016/S0021-9258(20)88238-6
  10. 10.1128/jb.175.12.3856-3862.1993
  11. 10.1128/jb.151.3.1279-1289.1982
  12. 10.1128/jb.138.1.118-121.1979
  13. D’Agnolo G. Rosenfeld I. S. Awaya J. Omura S. Vagelos P. R. Inhibition of fatty acid synthesis by the antibiotic cerulenin. Specific inactivation of beta-ketoacyl-acyl carrier protein synthetase.Biochim. Biophys. Acta3261973155166 (10.1016/0005-2760(73)90241-5) / Biochim. Biophys. Acta / Inhibition of fatty acid synthesis by the antibiotic cerulenin. Specific inactivation of beta-ketoacyl-acyl carrier protein synthetase by D’Agnolo G. (1973)
  14. Davis R. W. Botstein D. Roth J. R. Advanced bacterial genetics: a manual for genetic engineering. 1980 Cold Spring Harbor Laboratory Cold Spring Harbor N.Y
  15. Eberhard A. Burlingame A. L. Eberhard C. Kenyon G. L. Nealson K. H. Oppenheimer N. J. Structural identification of autoinducer of Photobacterium fischeri luciferase.Biochemistry20198124442449 (10.1021/bi00512a013) / Biochemistry / Structural identification of autoinducer of Photobacterium fischeri luciferase by Eberhard A. (1981)
  16. Eberhard A. Longin T. Widrig C. A. Stranick S. J. Synthesis of the lux gene autoinducer in Vibrio fischeri is positively autoregulated.Arch. Microbiol.1551991294297 (10.1007/BF00252215) / Arch. Microbiol. / Synthesis of the lux gene autoinducer in Vibrio fischeri is positively autoregulated by Eberhard A. (1991)
  17. Eberl L. Winson M. K. Sternberg C. Stewart G. S. A. B. Christiansen G. Chhabra S. R. Bycroft B. W. Williams P. Molin S. Givskov M. Involvement of N-acyl-l-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens.Mol. Microbiol.201996127136 (10.1111/j.1365-2958.1996.tb02495.x) / Mol. Microbiol. / Involvement of N-acyl-l-homoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens by Eberl L. (1996)
  18. Engebrecht J. Silverman M. Identification of genes and gene products necessary for bacterial bioluminescence.Proc. Natl. Acad. Sci. USA81198441544158 (10.1073/pnas.81.13.4154) / Proc. Natl. Acad. Sci. USA / Identification of genes and gene products necessary for bacterial bioluminescence by Engebrecht J. (1984)
  19. Fedorova N. D. Peredelchuk M. Y. Kirpichnikov M. P. Bennett G. N. Escherichia coli strain for thermoinducible T7 RNA polymerase-driven expression.Gene1771996267268 (10.1016/0378-1119(96)00294-6) / Gene / Escherichia coli strain for thermoinducible T7 RNA polymerase-driven expression by Fedorova N. D. (1996)
  20. 10.1146/annurev.micro.50.1.727
  21. Gellert M. Mizuuchi K. O’Dea M. H. Itoh T. Tomizawa J.-I. Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity.Proc. Natl. Acad. Sci. USA74197747724776 (10.1073/pnas.74.11.4772) / Proc. Natl. Acad. Sci. USA / Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity by Gellert M. (1977)
  22. 10.1128/jb.177.23.6946-6951.1995
  23. Gold M. Hausmann R. Maitra U. Hurwitz J. The enzymatic methylation of RNA and DNA. VIII. Effects of bacteriophage infection on the activity of the methylating enzymes.Proc. Natl. Acad. Sci. USA521964292297 (10.1073/pnas.52.2.292) / Proc. Natl. Acad. Sci. USA / The enzymatic methylation of RNA and DNA. VIII. Effects of bacteriophage infection on the activity of the methylating enzymes by Gold M. (1964)
  24. Grana D. Gardella T. Susskind M. M. The effects of mutations in the ant promoter of phage P22 depend on context.Genetics1201988319327 (10.1093/genetics/120.2.319) / Genetics / The effects of mutations in the ant promoter of phage P22 depend on context by Grana D. (1988)
  25. Grassberger M. A. Turnowsky F. Hildebrandt J. Preparation and antibacterial activities of new 1,2,3-diazaborine derivatives and analogues.J. Med. Chem.271984947953 (10.1021/jm00374a003) / J. Med. Chem. / Preparation and antibacterial activities of new 1,2,3-diazaborine derivatives and analogues by Grassberger M. A. (1984)
  26. 10.1128/jb.178.17.5291-5294.1996
  27. 10.1128/jb.98.2.559-567.1969
  28. Henry M. F. Cronan J. E. Jr. Escherichia coli transcription factor that both activates fatty acid synthesis and represses fatty acid degradation.J. Mol. Biol.2221991843849 (10.1016/0022-2836(91)90574-P) / J. Mol. Biol. / Escherichia coli transcription factor that both activates fatty acid synthesis and represses fatty acid degradation by Henry M. F. (1991)
  29. 10.1128/jb.169.8.3625-3632.1987
  30. Hwang I. Li P. L. Zhang L. Piper K. R. Cook D. M. Tate M. E. Farrand S. K. TraI, a LuxI homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer.Proc. Natl. Acad. Sci. USA91199446394643 (10.1073/pnas.91.11.4639) / Proc. Natl. Acad. Sci. USA / TraI, a LuxI homologue, is responsible for production of conjugation factor, the Ti plasmid N-acylhomoserine lactone autoinducer by Hwang I. (1994)
  31. Kaplan H. B. Greenberg E. P. Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system.J. Bacteriol.1631985210214 (10.1128/jb.163.3.1210-1214.1985) / J. Bacteriol. / Diffusion of autoinducer is involved in regulation of the Vibrio fischeri luminescence system by Kaplan H. B. (1985)
  32. Klein K. Steinberg R. Fiethen B. Overath P. Fatty acid degradation in Escherichia coli. An inducible system for the uptake of fatty acids and further characterization of old mutants.Eur. J. Biochem.191971442450 (10.1111/j.1432-1033.1971.tb01334.x) / Eur. J. Biochem. / Fatty acid degradation in Escherichia coli. An inducible system for the uptake of fatty acids and further characterization of old mutants by Klein K. (1971)
  33. Knoll L. J. Gordon J. I. Use of strains containing fad mutations plus a triple plasmid system to study import of myristate, its activation by Saccharomyces cerevisiae acyl-CoA synthetase and its utilization by S. cerevisiae myristoyl-CoA-protein N-myristoyltransferase.J. Biol. Chem.268199342814290 (10.1016/S0021-9258(18)53607-3) / J. Biol. Chem. / Use of strains containing fad mutations plus a triple plasmid system to study import of myristate, its activation by Saccharomyces cerevisiae acyl-CoA synthetase and its utilization by S. cerevisiae myristoyl-CoA-protein N-myristoyltransferase by Knoll L. J. (1993)
  34. Lombardini J. Coulter A. W. Talalay P. Analogues of methionine as substrates and inhibitors of the methionine adenosyltransferase reaction.Mol. Pharmacol.61970481499 / Mol. Pharmacol. / Analogues of methionine as substrates and inhibitors of the methionine adenosyltransferase reaction by Lombardini J. (1970)
  35. 10.1128/mr.57.3.522-542.1993
  36. 10.1006/jmbi.1996.0399
  37. Miyamoto C. M. Graham A. F. Meighen E. A. Nucleotide sequence of the luxC gene and the upstream DNA from the bioluminescent system of Vibrio harveyi.Nucleic Acids Res.16198815511562 (10.1093/nar/16.4.1551) / Nucleic Acids Res. / Nucleotide sequence of the luxC gene and the upstream DNA from the bioluminescent system of Vibrio harveyi by Miyamoto C. M. (1988)
  38. Moré M. I. Finger L. D. Stryker J. L. Fuqua C. Eberhard A. Winans S. C. Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates.Science272199616551658 (10.1126/science.272.5268.1655) / Science / Enzymatic synthesis of a quorum-sensing autoinducer through use of defined substrates by Moré M. I. (1996)
  39. 10.1128/jb.178.1.306-308.1996
  40. Overath P. Pauli G. Schairer H. U. Fatty acid degradation in Escherichia coli. An inducible acyl-CoA synthetase, the mapping of old mutations, and the isolation of regulatory mutants.Eur. J. Biochem.71969559574 (10.1111/j.1432-1033.1969.tb19644.x) / Eur. J. Biochem. / Fatty acid degradation in Escherichia coli. An inducible acyl-CoA synthetase, the mapping of old mutations, and the isolation of regulatory mutants by Overath P. (1969)
  41. Pearson J. P. Gray K. M. Passador L. Tucker K. D. Eberhard A. Iglewski B. A. Greenberg E. P. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes.Proc. Natl. Acad. Sci. USA911994197201 (10.1073/pnas.91.1.197) / Proc. Natl. Acad. Sci. USA / Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes by Pearson J. P. (1994)
  42. 10.1128/AAC.13.4.676
  43. Salmond G. P. Bycroft B. W. Stewart G. S. Williams P. The bacterial ’enigma’: cracking the code of cell-cell communication.Mol. Microbiol.161995615624 (10.1111/j.1365-2958.1995.tb02424.x) / Mol. Microbiol. / The bacterial ’enigma’: cracking the code of cell-cell communication by Salmond G. P. (1995)
  44. Sambrook J. Fritsch E. F. Maniatis T. Molecular cloning: a laboratory manual 2nd ed. 1989 Cold Spring Harbor Laboratory Cold Spring Harbor N.Y
  45. 10.1128/jb.172.8.4489-4496.1990
  46. Schaefer A. L. Val D. L. Hanzelka B. L. Cronan J. E. Jr. Greenberg E. P. Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein.Proc. Natl. Acad. Sci. USA93199695059509 (10.1073/pnas.93.18.9505) / Proc. Natl. Acad. Sci. USA / Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein by Schaefer A. L. (1996)
  47. Shaw P. D. Ping G. Daly S. L. Cha C. Cronan J. E. Jr. Rinehart K. L. Farrand S. K. Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography.Proc. Natl. Acad. Sci. USA94199760366041 (10.1073/pnas.94.12.6036) / Proc. Natl. Acad. Sci. USA / Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography by Shaw P. D. (1997)
  48. 10.1128/jb.142.2.621-632.1980
  49. 10.1128/jb.143.2.726-730.1980
  50. Steinbuchel A. Schlegel H. G. Physiology and molecular genetics of poly(β-hydroxyalkanoic acid) synthesis in Alcaligenes eutrophus.Mol. Microbiol.51991535542 (10.1111/j.1365-2958.1991.tb00725.x) / Mol. Microbiol. / Physiology and molecular genetics of poly(β-hydroxyalkanoic acid) synthesis in Alcaligenes eutrophus by Steinbuchel A. (1991)
  51. Studier F. W. Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system.J. Mol. Biol.21919913744 (10.1016/0022-2836(91)90855-Z) / J. Mol. Biol. / Use of bacteriophage T7 lysozyme to improve an inducible T7 expression system by Studier F. W. (1991)
  52. Sugino A. Peebles C. L. Kreuzer K. N. Cozzarelli N. R. Mechanism of action of nalidixic acid: purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme.Proc. Natl. Acad. Sci. USA74197747674771 (10.1073/pnas.74.11.4767) / Proc. Natl. Acad. Sci. USA / Mechanism of action of nalidixic acid: purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme by Sugino A. (1977)
  53. Sun W. Cao J.-G. Teng K. Meighen E. A. Biosynthesis of poly-3-hydroxybutyrate in the luminescent bacterium, Vibrio harveyi, and regulation by the lux autoinducer N-(3-hydroxybutanoyl)homoserine lactone.J. Biol. Chem.26919942078520790 (10.1016/S0021-9258(17)32061-6) / J. Biol. Chem. / Biosynthesis of poly-3-hydroxybutyrate in the luminescent bacterium, Vibrio harveyi, and regulation by the lux autoinducer N-(3-hydroxybutanoyl)homoserine lactone by Sun W. (1994)
  54. 10.1128/jb.117.1.133-143.1974
  55. 10.1128/jb.118.3.990-998.1974
  56. Throup J. P. Camara M. Briggs G. S. Winson M. K. Chhabra S. R. Bycroft B. W. Williams P. Stewart G. S. A. B. Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules.Mol. Microbiol.171995345356 (10.1111/j.1365-2958.1995.mmi_17020345.x) / Mol. Microbiol. / Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules by Throup J. P. (1995)
  57. 10.1128/jb.171.12.6555-6565.1989
  58. Val D. L. Chapman-Smith A. Walker M. E. Cronan J. E. Wallace J. C. Polymorphism of the yeast pyruvate carboxylase 2 gene and protein: effects on protein biotinylation.Biochem. J.3121995817825 (10.1042/bj3120817) / Biochem. J. / Polymorphism of the yeast pyruvate carboxylase 2 gene and protein: effects on protein biotinylation by Val D. L. (1995)
  59. Vance D. Goldberg I. Mitsuhashi O. Bloch K. Omura S. Nomura S. Inhibition of fatty acid synthetases by the antibiotic cerulenin.Biochem. Biophys. Res. Commun.481972649656 (10.1016/0006-291X(72)90397-X) / Biochem. Biophys. Res. Commun. / Inhibition of fatty acid synthetases by the antibiotic cerulenin by Vance D. (1972)
  60. 10.1128/jb.97.2.827-836.1969
  61. Woldringh C. L. Nanninga N. Structure of the nucleoid and cytoplasm in the intact cell Molecular cytology of Escherichia coli. Naninga N. 1985 161 198 Academic Press Orlando Fla
  62. 10.1016/0378-1119(85)90120-9
  63. Zhang L. Murphy P. J. Kerr A. Tate M. E. Agrobacterium conjugation and gene regulation by N-acyl-l-homoserine lactones.Nature3621993446448 (10.1038/362446a0) / Nature / Agrobacterium conjugation and gene regulation by N-acyl-l-homoserine lactones by Zhang L. (1993)
Dates
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Created 5 years, 8 months ago (Dec. 31, 2019, 11:23 a.m.)
Deposited 4 years, 1 month ago (July 29, 2021, 2:20 p.m.)
Indexed 3 months, 2 weeks ago (May 21, 2025, 9:29 a.m.)
Issued 27 years, 3 months ago (May 15, 1998)
Published 27 years, 3 months ago (May 15, 1998)
Published Print 27 years, 3 months ago (May 15, 1998)
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@article{Val_1998, title={In Vivo Evidence that S -Adenosylmethionine and Fatty Acid Synthesis Intermediates Are the Substrates for the LuxI Family of Autoinducer Synthases}, volume={180}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.180.10.2644-2651.1998}, DOI={10.1128/jb.180.10.2644-2651.1998}, number={10}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Val, Dale L. and Cronan, John E.}, year={1998}, month=may, pages={2644–2651} }