Abstract
In Vibrio fischeri, the synthesis of N-3-oxohexanoyl-L-homoserine lactone, the autoinducer for population density-responsive induction of the luminescence operon (the lux operon, luxICDABEG), is dependent on the autoinducer synthase gene luxI. Gene replacement mutants of V. fischeri defective in luxI, which had been expected to produce no autoinducer, nonetheless exhibited lux operon transcriptional activation. Mutants released into the medium a compound that, like N-3-oxohexanoyl-L-homoserine lactone, activated expression of the lux system in a dose-dependent manner and was both extractable with ethyl acetate and labile to base. The luxI-independent compound, also like N-3-oxohexanoyl-L-homoserine lactone, was produced by V. fischeri cells in a regulated, population density-responsive manner and required the transcriptional activator LuxR for activity in the lux system. The luxI-independent compound was identified as N-octanoyl-L-homoserine lactone by coelution with the synthetic compound in reversed-phase high-pressure liquid chromatography, by derivatization treatment with 2,4-dinitrophenylhydrazine, by mass spectrometry, and by nuclear magnetic resonance spectroscopy. A locus, ain, necessary and sufficient for Escherichia coli to synthesize N-octanoyl-L-homoserine lactone was cloned from the V. fischeri genome and found to be distinct from luxI by restriction mapping and Southern hybridization. N-Octanoyl-L-homoserine lactone and ain constitute a second, novel autoinduction system for population density-responsive signalling and regulation of lux gene expression, and possibly other genes, in V. fischeri. A third V. fischeri autoinducer, N-hexanoyl-L-homoserine lactone, dependent on luxI for its synthesis, was also identified. The presence of multiple chemically and genetically distinct but cross-acting autoinduction systems in V. fischeri indicates unexpected complexity for autoinduction as a regulatory mechanism in this bacterium.
References
32
Referenced
137
- Ausubel F. M. R. Brent R. E. Kingston D. D. Moore J. A. Smith J. G. Seidman and K. Struhl. 1987. Current protocols in molecular biology. John Wiley New York.
-
Bainton , N. J. , P. Stead , S. R. Chhabra , B. W. Bycroft , G. P. C. Salmond , G. S. A. B. Stewart , and P. Williams . 1992 . N-(3-Oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotova . Biochem. J. 288 : 997 - 1004 .
(
10.1042/bj2880997
) / Biochem. J. / N-(3-Oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotova by Bainton N. J. (1992) -
Bassler , B. L. , M. Wright , R. E. Showalter , and M. R Silverman . 1993 . Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of Iuminescence. Mol. Microbiol. 9 : 773 - 786 .
(
10.1111/j.1365-2958.1993.tb01737.x
) / Iuminescence. Mol. Microbiol. / Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of by Bassler B. L. (1993) -
Cao , J. , and E. A. Meighen . 1989 . Purification and structural identification of an autoinducer for the Iuminescence system of Vibrio harveyi . J. Biol. Chem. 264 : 21670 - 21676 .
(
10.1016/S0021-9258(20)88238-6
) / J. Biol. Chem. / Purification and structural identification of an autoinducer for the Iuminescence system of Vibrio harveyi by Cao J. (1989) -
Dunlap , P. V. 1992 . Mechanism for iron control of the Vibio fischeri Iuminescence system: involvement of cyclic AMP and cyclic AMP receptor protein and modulation of DNA level . J. Biolumin. Chemilumin. 7 : 203 - 214 .
(
10.1002/bio.1170070307
) / J. Biolumin. Chemilumin. / Mechanism for iron control of the Vibio fischeri Iuminescence system: involvement of cyclic AMP and cyclic AMP receptor protein and modulation of DNA level by Dunlap P. V. (1992) -
Dunlap , P. V. , and S. M. Callahan . 1993 . Characterization of a periplasmic 3':5'-cyclic nucleotide phosphodiesterase gene, cpdP, from the marine symbiotic bacterium Vibrio fischeri . J. Bacteriol. 175 : 4615 - 4624 .
(
10.1128/jb.175.15.4615-4624.1993
) / J. Bacteriol. / Characterization of a periplasmic 3':5'-cyclic nucleotide phosphodiesterase gene, cpdP, from the marine symbiotic bacterium Vibrio fischeri by Dunlap P. V. (1993) -
Dunlap , P. V. , and E. P. Greenberg . 1988 . Control of Vibriofischeri lux gene transcription by a cyclic AMP receptor protein-LuxR protein regulatory circuit . J. Bacteriol. 170 : 40404046 .
(
10.1128/jb.170.9.4040-4046.1988
) / J. Bacteriol. / Control of Vibriofischeri lux gene transcription by a cyclic AMP receptor protein-LuxR protein regulatory circuit by Dunlap P. V. (1988) -
Dunlap , P. V. , and A. KUo. 1992 . Cell density-dependent modulation of the Vibrio fischeri Iuminescence system in the absence of autoinducer and LuxR protein . J. Bacteriol. 174 : 2440 - 2448 .
(
10.1128/jb.174.8.2440-2448.1992
) / J. Bacteriol. / Cell density-dependent modulation of the Vibrio fischeri Iuminescence system in the absence of autoinducer and LuxR protein by Dunlap P. V. (1992) -
Dunlap , P. V. , and J. M. Ray . 1989 . Requirement for autoinducer in transcriptional negative autoregulation of the Vbrio fischeri luxR gene in Escherichia coli . J. Bacteriol. 171 : 3549 - 3552 .
(
10.1128/jb.171.6.3549-3552.1989
) / J. Bacteriol. / Requirement for autoinducer in transcriptional negative autoregulation of the Vbrio fischeri luxR gene in Escherichia coli by Dunlap P. V. (1989) -
Eberhard , A. , A. L. Burlingame , C. Eberhard , G. L. Kenyon , K. H. Nealson , and N. J. Oppenheimer . 1981 . Structural identification of autoinducer of Photobactenium fischeri Iuciferase . Biochemistry 20 : 2444 - 2449 .
(
10.1021/bi00512a013
) / Biochemistry / Structural identification of autoinducer of Photobactenium fischeri Iuciferase by Eberhard A. (1981) -
Eberhard , A. , T. Longin , C. A. Widrig , and S. J. Stranick 1991 . Synthesis of the Iux gene autoinducer in Vibriofischeri is positively autoregulated . Arch. Microbiol. 155 : 294 - 297 .
(
10.1007/BF00252215
) / Arch. Microbiol. / Synthesis of the Iux gene autoinducer in Vibriofischeri is positively autoregulated by Eberhard A. (1991) -
Eberhard , A. , C. A. Widrig , P. McBath , and J. B. Schineller . 1986 . Analogs of the autoinducer of bioluminescence in Vibrio fischeri . Arch. Microbiol. 146 : 3540 .
(
10.1007/BF00690155
) / Arch. Microbiol. / Analogs of the autoinducer of bioluminescence in Vibrio fischeri by Eberhard A. (1986) -
Engebrecht , J. , K. Nealson , and M. Silverman . 1983 . Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri . Cell 32 : 773 - 781 .
(
10.1016/0092-8674(83)90063-6
) / Cell / Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri by Engebrecht J. (1983) -
Engebrecht , J. , and M. Silverman . 1984 . Identification of genes and gene products necessary for bacterial bioluminescence . Proc. Natl. Acad. Sci. USA 81 : 4154 - 4158 .
(
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) -
Friedrich , W. F. , and E. P. Greenberg . 1983 . Glucose repression of luminescence and Iuciferase in Vibrio fischeri . Arch. Microbiol. 134 : 87 - 91 .
(
10.1007/BF00407937
) / Arch. Microbiol. / Glucose repression of luminescence and Iuciferase in Vibrio fischeri by Friedrich W. F. (1983) -
Fuqua , W. C. , and S. C. Winans . 1994 . A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite . J. Bacteriol. 176 : 2796 - 2806 .
(
10.1128/jb.176.10.2796-2806.1994
) / J. Bacteriol. / A LuxR-LuxI type regulatory system activates Agrobacterium Ti plasmid conjugal transfer in the presence of a plant tumor metabolite by Fuqua W. C. (1994) -
Gambello , M. J. , and B. H. Iglewski . 1991 . Cloning and characterization of the Pseudomonas aeruginosa IasR gene, a transcriptional activator of elastase expression . J. Bacteriol. 173 : 3000 - 3009 .
(
10.1128/jb.173.9.3000-3009.1991
) / J. Bacteriol. / Cloning and characterization of the Pseudomonas aeruginosa IasR gene, a transcriptional activator of elastase expression by Gambello M. J. (1991) - Gilson L. A. Kuo and P. V. Dunlap. Unpublished data.
-
Huisman , G. W. , and R Kolter . 1994 . Sensing starvation: a homoserine lactone-dependent signalling pathway in Escherichia coli . Science 265 : 537 - 539 .
(
10.1126/science.7545940
) / Science / Sensing starvation: a homoserine lactone-dependent signalling pathway in Escherichia coli by Huisman G. W. (1994) -
Kaplan , H. B. , and E. P. Greenberg . 1985 . Diffusion of autoinducer is involved in regulation of the Vibriofischeri Iuminescence system . J. Bacteriol. 163 : 1210 - 1214 .
(
10.1128/jb.163.3.1210-1214.1985
) / J. Bacteriol. / Diffusion of autoinducer is involved in regulation of the Vibriofischeri Iuminescence system by Kaplan H. B. (1985) -
Kieber , D. J. , and N. V. Blough . 1990 . Determination of carboncentered radicals in aqueous solution by liquid chromatography with fluorescence detection . Anal. Chem. 62 : 2275 - 2283 .
(
10.1021/ac00220a005
) / Anal. Chem. / Determination of carboncentered radicals in aqueous solution by liquid chromatography with fluorescence detection by Kieber D. J. (1990) -
Kieber , D. J. , and K. Mopper . 1986 . Trace determination of cr-keto acids in natural waters . Anal. Chim. Acta 183 : 129 - 140 .
(
10.1016/0003-2670(86)80081-2
) / Anal. Chim. Acta / Trace determination of cr-keto acids in natural waters by Kieber D. J. (1986) - Nealson K. H. and J. W. Hastings. 1992. The Iuminous bacteria p. 625-639. In A. Balows H. G. Truper M. Dworkin W. Harder and K-H. Schleifer (ed.) The prokaryotes 2nd ed. Springer-Verlag Berlin.
-
Passador , L. , J. M. Cook , M. J. Gambello , L. Rust , and B. H. Iglewski . 1993 . Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication . Science 260 : 1127 - 1130 .
(
10.1126/science.8493556
) / Science / Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication by Passador L. (1993) -
Pearson , J. P. , K. M. Gray , L. Passador , K. D. Tucker , A. Eberhard , B. H. Iglewski , and E. P. Greenberg . 1994 . Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes . Proc. Natl. Acad. Sci. USA 91 : 197 - 201 .
(
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) -
Piper , K R . , S. B. von Bodman , and S. K. Farrand . 1993 . Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction . Nature (London) 362 : 448 - 450 .
(
10.1038/362448a0
) / Nature (London) / Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction by Piper K R (1993) -
Pirhonen , M. , D. Flego , R Heikinheimo , and E. T. Palva . 1993 . A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora . EMBO J. 12 : 2467 - 2476 .
(
10.1002/j.1460-2075.1993.tb05901.x
) / EMBO J. / A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora by Pirhonen M. (1993) -
Ruby , E. G. , and K. H. Nealson . 1976 . Symbiotic association of Photobacterium fischeri with the marine Iuminous fish Monocentris japonica: a model of symbiosis based on bacterial studies . Biol. Bull. (Woods Hole) 141 : 574 - 586 .
(
10.2307/1540507
) / Biol. Bull. (Woods Hole) / Symbiotic association of Photobacterium fischeri with the marine Iuminous fish Monocentris japonica: a model of symbiosis based on bacterial studies by Ruby E. G. (1976) -
Simon , R. , M. O'Connell , M. Labes , and A. Puihler . 1986 . Plasmid vectors for the genetic analysis and manipulation of rhizobia and other gram-negative bacteria . Methods Enzymol. 118 : 640 - 659 .
(
10.1016/0076-6879(86)18106-7
) / Methods Enzymol. / Plasmid vectors for the genetic analysis and manipulation of rhizobia and other gram-negative bacteria by Simon R. (1986) -
Swartzman , E. , S. Kapoor , A. F. Graham , and E. A. Meighen . 1990 . A new Vibrio fischeni Iux gene precedes a bidirectional termination site for the Iux operon . J. Bacteriol. 172 : 6797 - 6802 .
(
10.1128/jb.172.12.6797-6802.1990
) / J. Bacteriol. / A new Vibrio fischeni Iux gene precedes a bidirectional termination site for the Iux operon by Swartzman E. (1990) -
Yanisch-Perron , C. , J. Vieira , and J. Messing . 1985 . Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl 8 and pUC19 vectors . Gene 33 : 103 - 119 .
(
10.1016/0378-1119(85)90120-9
) / Gene / Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl 8 and pUC19 vectors by Yanisch-Perron C. (1985) -
Zhang , L , P. J. Murphy , A. Kerr , and M. E. Tate . 1993 . Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones . Nature (London) 362 : 446 - 448 .
(
10.1038/362446a0
) / Nature (London) / Agrobacterium conjugation and gene regulation by N-acyl-L-homoserine lactones by Zhang L (1993)
Dates
Type | When |
---|---|
Created | 8 years, 9 months ago (Nov. 7, 2016, 4:37 p.m.) |
Deposited | 4 years, 1 month ago (July 29, 2021, 1:20 p.m.) |
Indexed | 1 month ago (Aug. 5, 2025, 8:22 a.m.) |
Issued | 30 years, 9 months ago (Dec. 1, 1994) |
Published | 30 years, 9 months ago (Dec. 1, 1994) |
Published Print | 30 years, 9 months ago (Dec. 1, 1994) |
@article{Kuo_1994, title={Multiple N-acyl-L-homoserine lactone autoinducers of luminescence in the marine symbiotic bacterium Vibrio fischeri}, volume={176}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.176.24.7558-7565.1994}, DOI={10.1128/jb.176.24.7558-7565.1994}, number={24}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Kuo, A and Blough, N V and Dunlap, P V}, year={1994}, month=dec, pages={7558–7565} }