Europe PMC
Nothing Special   »   [go: up one dir, main page]

Europe PMC requires Javascript to function effectively.

Either your web browser doesn't support Javascript or it is currently turned off. In the latter case, please turn on Javascript support in your web browser and reload this page.

This website requires cookies, and the limited processing of your personal data in order to function. By using the site you are agreeing to this as outlined in our privacy notice and cookie policy.

Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules.

Author information

Affiliations

  • 1. Department of Applied Biochemistry and Food Science, University of Nottingham, Leicestershire, United Kingdom.
      Authors
    • Swift S 1
    (1 author)

ORCIDs linked to this article

Journal of Bacteriology, 01 Sep 1997, 179(17):5271-5281
https://doi.org/10.1128/jb.179.17.5271-5281.1997 PMID: 9286976 PMCID: PMC179392

Free full text in Europe PMC

Abstract 

Spent culture supernatants from both Aeromonas hydrophila and Aeromonas salmonicida activate a range of biosensors responsive to N-acylhomoserine lactones (AHLs). The genes for a quorum sensing signal generator and a response regulator were cloned from each Aeromonas species and termed ahyRI and asaRI, respectively. Protein sequence homology analysis places the gene products within the growing family of LuxRI homologs. ahyR and asaR are transcribed divergently from ahyI and asaI, respectively, and in both Aeromonas species, the genes downstream have been identified by DNA sequence and PCR analysis. Downstream of both ahyI and asaI is a gene with close homology to iciA, an inhibitor of chromosome replication in Escherichia coli, a finding which implies that in Aeromonas, cell division may be linked to quorum sensing. The major signal molecule synthesized via both AhyI and AsaI was purified from spent culture supernatants and identified as N-(butanoyl)-L-homoserine lactone (BHL) by thin-layer chromatography, high-pressure liquid chromatography analysis, and mass spectrometry. In addition, a second, minor AHL, N-hexanoyl-L-homoserine lactone, was identified. Transcriptional reporter studies with ahyI::luxCDABE fusions indicate that AhyR and BHL are both required for ahyI transcription. For A. salmonicida, although the addition of exogenous BHL gives only a small stimulation of the production of serine protease with comparison to the control culture, the incorporation of a longer-chain AHL, N-(3-oxodecanoyl)-L-homoserine lactone, reduced the final level (by approximately 50%) and delayed the appearance (from an A650 of 0.9 in the control to an A650 of 1.2 in the test) of protease in the culture supernatant. These data add A. hydrophila and A. salmonicida to the growing family of gram-negative bacteria now known to control gene expression through quorum sensing.

Free full text 

Logo of jbacterLink to Publisher's site
J Bacteriol. 1997 Sep; 179(17): 5271–5281.
PMCID: PMC179392
PMID: 9286976

Quorum sensing in Aeromonas hydrophila and Aeromonas salmonicida: identification of the LuxRI homologs AhyRI and AsaRI and their cognate N-acylhomoserine lactone signal molecules.

S Swift, A V Karlyshev, L Fish, E L Durant, M K Winson, S R Chhabra, P Williams, S Macintyre, and G S Stewart
Author information Copyright and License information Disclaimer
Abstract

Spent culture supernatants from both Aeromonas hydrophila and Aeromonas salmonicida activate a range of biosensors responsive to N-acylhomoserine lactones (AHLs). The genes for a quorum sensing signal generator and a response regulator were cloned from each Aeromonas species and termed ahyRI and asaRI, respectively. Protein sequence homology analysis places the gene products within the growing family of LuxRI homologs. ahyR and asaR are transcribed divergently from ahyI and asaI, respectively, and in both Aeromonas species, the genes downstream have been identified by DNA sequence and PCR analysis. Downstream of both ahyI and asaI is a gene with close homology to iciA, an inhibitor of chromosome replication in Escherichia coli, a finding which implies that in Aeromonas, cell division may be linked to quorum sensing. The major signal molecule synthesized via both AhyI and AsaI was purified from spent culture supernatants and identified as N-(butanoyl)-L-homoserine lactone (BHL) by thin-layer chromatography, high-pressure liquid chromatography analysis, and mass spectrometry. In addition, a second, minor AHL, N-hexanoyl-L-homoserine lactone, was identified. Transcriptional reporter studies with ahyI::luxCDABE fusions indicate that AhyR and BHL are both required for ahyI transcription. For A. salmonicida, although the addition of exogenous BHL gives only a small stimulation of the production of serine protease with comparison to the control culture, the incorporation of a longer-chain AHL, N-(3-oxodecanoyl)-L-homoserine lactone, reduced the final level (by approximately 50%) and delayed the appearance (from an A650 of 0.9 in the control to an A650 of 1.2 in the test) of protease in the culture supernatant. These data add A. hydrophila and A. salmonicida to the growing family of gram-negative bacteria now known to control gene expression through quorum sensing.

Full Text
The Full Text of this article is available as a PDF (812K).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
  • Akrim M, Bally M, Ball G, Tommassen J, Teerink H, Filloux A, Lazdunski A. Xcp-mediated protein secretion in Pseudomonas aeruginosa: identification of two additional genes and evidence for regulation of xcp gene expression. Mol Microbiol. 1993 Oct;10(2):431–443. [Abstract] [Google Scholar]
  • Anguita J, Rodríguez Aparicio LB, Naharro G. Purification, gene cloning, amino acid sequence analysis, and expression of an extracellular lipase from an Aeromonas hydrophila human isolate. Appl Environ Microbiol. 1993 Aug;59(8):2411–2417. [Europe PMC free article] [Abstract] [Google Scholar]
  • Bainton NJ, Stead P, Chhabra SR, Bycroft BW, Salmond GP, Stewart GS, Williams P. N-(3-oxohexanoyl)-L-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem J. 1992 Dec 15;288(Pt 3):997–1004. [Europe PMC free article] [Abstract] [Google Scholar]
  • Bartolomé B, Jubete Y, Martínez E, de la Cruz F. Construction and properties of a family of pACYC184-derived cloning vectors compatible with pBR322 and its derivatives. Gene. 1991 Jun 15;102(1):75–78. [Abstract] [Google Scholar]
  • Bassler BL, Wright M, Silverman MR. Sequence and function of LuxO, a negative regulator of luminescence in Vibrio harveyi. Mol Microbiol. 1994 May;12(3):403–412. [Abstract] [Google Scholar]
  • Braun V, Schmitz G. Excretion of a protease by Serratia marcescens. Arch Microbiol. 1980 Jan;124(1):55–61. [Abstract] [Google Scholar]
  • Cui Y, Chatterjee A, Liu Y, Dumenyo CK, Chatterjee AK. Identification of a global repressor gene, rsmA, of Erwinia carotovora subsp. carotovora that controls extracellular enzymes, N-(3-oxohexanoyl)-L-homoserine lactone, and pathogenicity in soft-rotting Erwinia spp. J Bacteriol. 1995 Sep;177(17):5108–5115. [Europe PMC free article] [Abstract] [Google Scholar]
  • Chatterjee A, Cui Y, Liu Y, Dumenyo CK, Chatterjee AK. Inactivation of rsmA leads to overproduction of extracellular pectinases, cellulases, and proteases in Erwinia carotovora subsp. carotovora in the absence of the starvation/cell density-sensing signal, N-(3-oxohexanoyl)-L-homoserine lactone. Appl Environ Microbiol. 1995 May;61(5):1959–1967. [Europe PMC free article] [Abstract] [Google Scholar]
  • Chhabra SR, Stead P, Bainton NJ, Salmond GP, Stewart GS, Williams P, Bycroft BW. Autoregulation of carbapenem biosynthesis in Erwinia carotovora by analogues of N-(3-oxohexanoyl)-L-homoserine lactone. J Antibiot (Tokyo) 1993 Mar;46(3):441–454. [Abstract] [Google Scholar]
  • Choi SH, Greenberg EP. Genetic dissection of DNA binding and luminescence gene activation by the Vibrio fischeri LuxR protein. J Bacteriol. 1992 Jun;174(12):4064–4069. [Europe PMC free article] [Abstract] [Google Scholar]
  • de Lorenzo V, Herrero M, Jakubzik U, Timmis KN. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J Bacteriol. 1990 Nov;172(11):6568–6572. [Europe PMC free article] [Abstract] [Google Scholar]
  • Devereux J, Haeberli P, Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. [Europe PMC free article] [Abstract] [Google Scholar]
  • Devine JH, Shadel GS, Baldwin TO. Identification of the operator of the lux regulon from the Vibrio fischeri strain ATCC7744. Proc Natl Acad Sci U S A. 1989 Aug;86(15):5688–5692. [Europe PMC free article] [Abstract] [Google Scholar]
  • Eberhard A, Burlingame AL, Eberhard C, Kenyon GL, Nealson KH, Oppenheimer NJ. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry. 1981 Apr 28;20(9):2444–2449. [Abstract] [Google Scholar]
  • Eberl L, Winson MK, Sternberg C, Stewart GS, Christiansen G, Chhabra SR, Bycroft B, Williams P, Molin S, Givskov M. Involvement of N-acyl-L-hormoserine lactone autoinducers in controlling the multicellular behaviour of Serratia liquefaciens. Mol Microbiol. 1996 Apr;20(1):127–136. [Abstract] [Google Scholar]
  • Engebrecht J, Nealson K, Silverman M. Bacterial bioluminescence: isolation and genetic analysis of functions from Vibrio fischeri. Cell. 1983 Mar;32(3):773–781. [Abstract] [Google Scholar]
  • Frohman MA, Dush MK, Martin GR. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. [Europe PMC free article] [Abstract] [Google Scholar]
  • Fuqua C, Winans SC, Greenberg EP. Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. Annu Rev Microbiol. 1996;50:727–751. [Abstract] [Google Scholar]
  • Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria: the LuxR-LuxI family of cell density-responsive transcriptional regulators. J Bacteriol. 1994 Jan;176(2):269–275. [Europe PMC free article] [Abstract] [Google Scholar]
  • García-Lara J, Shang LH, Rothfield LI. An extracellular factor regulates expression of sdiA, a transcriptional activator of cell division genes in Escherichia coli. J Bacteriol. 1996 May;178(10):2742–2748. [Europe PMC free article] [Abstract] [Google Scholar]
  • Gilson L, Kuo A, Dunlap PV. AinS and a new family of autoinducer synthesis proteins. J Bacteriol. 1995 Dec;177(23):6946–6951. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hanzelka BL, Greenberg EP. Evidence that the N-terminal region of the Vibrio fischeri LuxR protein constitutes an autoinducer-binding domain. J Bacteriol. 1995 Feb;177(3):815–817. [Europe PMC free article] [Abstract] [Google Scholar]
  • Hastings JW, Nealson KH. Bacterial bioluminescence. Annu Rev Microbiol. 1977;31:549–595. [Abstract] [Google Scholar]
  • Hill PJ, Swift S, Stewart GS. PCR based gene engineering of the Vibrio harveyi lux operon and the Escherichia coli trp operon provides for biochemically functional native and fused gene products. Mol Gen Genet. 1991 Apr;226(1-2):41–48. [Abstract] [Google Scholar]
  • Hwang I, Cook DM, Farrand SK. A new regulatory element modulates homoserine lactone-mediated autoinduction of Ti plasmid conjugal transfer. J Bacteriol. 1995 Jan;177(2):449–458. [Europe PMC free article] [Abstract] [Google Scholar]
  • Janda JM. Recent advances in the study of the taxonomy, pathogenicity, and infectious syndromes associated with the genus Aeromonas. Clin Microbiol Rev. 1991 Oct;4(4):397–410. [Europe PMC free article] [Abstract] [Google Scholar]
  • Jones S, Yu B, Bainton NJ, Birdsall M, Bycroft BW, Chhabra SR, Cox AJ, Golby P, Reeves PJ, Stephens S, et al. The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J. 1993 Jun;12(6):2477–2482. [Europe PMC free article] [Abstract] [Google Scholar]
  • Karlyshev AV, MacIntyre S. Cloning and study of the genetic organization of the exe gene cluster of Aeromonas salmonicida. Gene. 1995 May 26;158(1):77–82. [Abstract] [Google Scholar]
  • Latifi A, Foglino M, Tanaka K, Williams P, Lazdunski A. A hierarchical quorum-sensing cascade in Pseudomonas aeruginosa links the transcriptional activators LasR and RhIR (VsmR) to expression of the stationary-phase sigma factor RpoS. Mol Microbiol. 1996 Sep;21(6):1137–1146. [Abstract] [Google Scholar]
  • Latifi A, Winson MK, Foglino M, Bycroft BW, Stewart GS, Lazdunski A, Williams P. Multiple homologues of LuxR and LuxI control expression of virulence determinants and secondary metabolites through quorum sensing in Pseudomonas aeruginosa PAO1. Mol Microbiol. 1995 Jul;17(2):333–343. [Abstract] [Google Scholar]
  • Lindeberg M, Collmer A. Analysis of eight out genes in a cluster required for pectic enzyme secretion by Erwinia chrysanthemi: sequence comparison with secretion genes from other gram-negative bacteria. J Bacteriol. 1992 Nov;174(22):7385–7397. [Europe PMC free article] [Abstract] [Google Scholar]
  • Ljungh A, Wretlind B, Möllby R. Separation and characterization of enterotoxin and two haemolysins from Aeromonas hydrophila. Acta Pathol Microbiol Scand B. 1981 Dec;89(6):387–397. [Abstract] [Google Scholar]
  • MacIntyre S, Buckley JT. Presence of glycerophospholipid: cholesterol acyltransferase and phospholipase in culture supernatant of Aeromonas hydrophila. J Bacteriol. 1978 Aug;135(2):402–407. [Europe PMC free article] [Abstract] [Google Scholar]
  • MacIntyre S, Trust TJ, Buckley JT. Distribution of glycerophospholipid-cholesterol acyltransferase in selected bacterial species. J Bacteriol. 1979 Jul;139(1):132–136. [Europe PMC free article] [Abstract] [Google Scholar]
  • Merino S, Rubires X, Knochel S, Tomas JM. Emerging pathogens: Aeromonas spp. Int J Food Microbiol. 1995 Dec;28(2):157–168. [Abstract] [Google Scholar]
  • Milton DL, Hardman A, Camara M, Chhabra SR, Bycroft BW, Stewart GS, Williams P. Quorum sensing in Vibrio anguillarum: characterization of the vanI/vanR locus and identification of the autoinducer N-(3-oxodecanoyl)-L-homoserine lactone. J Bacteriol. 1997 May;179(9):3004–3012. [Europe PMC free article] [Abstract] [Google Scholar]
  • HELZ GE, OLEARY WM, PANOS C. Studies on the nutrition of Bacterium salmonicida. J Bacteriol. 1956 Nov;72(5):673–676. [Europe PMC free article] [Abstract] [Google Scholar]
  • Ochsner UA, Reiser J. Autoinducer-mediated regulation of rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 1995 Jul 3;92(14):6424–6428. [Europe PMC free article] [Abstract] [Google Scholar]
  • Ochsner UA, Koch AK, Fiechter A, Reiser J. Isolation and characterization of a regulatory gene affecting rhamnolipid biosurfactant synthesis in Pseudomonas aeruginosa. J Bacteriol. 1994 Apr;176(7):2044–2054. [Europe PMC free article] [Abstract] [Google Scholar]
  • Passador L, Cook JM, Gambello MJ, Rust L, Iglewski BH. Expression of Pseudomonas aeruginosa virulence genes requires cell-to-cell communication. Science. 1993 May 21;260(5111):1127–1130. [Abstract] [Google Scholar]
  • Pearson JP, Passador L, Iglewski BH, Greenberg EP. A second N-acylhomoserine lactone signal produced by Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1490–1494. [Europe PMC free article] [Abstract] [Google Scholar]
  • Pirhonen M, Flego D, Heikinheimo R, Palva ET. A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J. 1993 Jun;12(6):2467–2476. [Europe PMC free article] [Abstract] [Google Scholar]
  • Romeo T, Gong M, Liu MY, Brun-Zinkernagel AM. Identification and molecular characterization of csrA, a pleiotropic gene from Escherichia coli that affects glycogen biosynthesis, gluconeogenesis, cell size, and surface properties. J Bacteriol. 1993 Aug;175(15):4744–4755. [Europe PMC free article] [Abstract] [Google Scholar]
  • Saiki RK, Gelfand DH, Stoffel S, Scharf SJ, Higuchi R, Horn GT, Mullis KB, Erlich HA. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. [Abstract] [Google Scholar]
  • Salmond GP, Bycroft BW, Stewart GS, Williams P. The bacterial 'enigma': cracking the code of cell-cell communication. Mol Microbiol. 1995 May;16(4):615–624. [Abstract] [Google Scholar]
  • Schweizer HP. Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene. 1991 Jan 2;97(1):109–121. [Abstract] [Google Scholar]
  • Simon R, Quandt J, Klipp W. New derivatives of transposon Tn5 suitable for mobilization of replicons, generation of operon fusions and induction of genes in gram-negative bacteria. Gene. 1989 Aug 1;80(1):161–169. [Abstract] [Google Scholar]
  • Sitnikov DM, Schineller JB, Baldwin TO. Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction. Proc Natl Acad Sci U S A. 1996 Jan 9;93(1):336–341. [Europe PMC free article] [Abstract] [Google Scholar]
  • Swift S, Throup JP, Williams P, Salmond GP, Stewart GS. Quorum sensing: a population-density component in the determination of bacterial phenotype. Trends Biochem Sci. 1996 Jun;21(6):214–219. [Abstract] [Google Scholar]
  • Swift S, Winson MK, Chan PF, Bainton NJ, Birdsall M, Reeves PJ, Rees CE, Chhabra SR, Hill PJ, Throup JP, et al. A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR:LuxI superfamily in enteric bacteria. Mol Microbiol. 1993 Nov;10(3):511–520. [Abstract] [Google Scholar]
  • Thöny B, Hwang DS, Fradkin L, Kornberg A. iciA, an Escherichia coli gene encoding a specific inhibitor of chromosomal initiation of replication in vitro. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4066–4070. [Europe PMC free article] [Abstract] [Google Scholar]
  • Throup JP, Camara M, Briggs GS, Winson MK, Chhabra SR, Bycroft BW, Williams P, Stewart GS. Characterisation of the yenI/yenR locus from Yersinia enterocolitica mediating the synthesis of two N-acylhomoserine lactone signal molecules. Mol Microbiol. 1995 Jul;17(2):345–356. [Abstract] [Google Scholar]
  • Whitby PW, Landon M, Coleman G. The cloning and nucleotide sequence of the serine protease gene (aspA) of Aeromonas salmonicida ssp. salmonicida. FEMS Microbiol Lett. 1992 Nov 15;78(1):65–71. [Abstract] [Google Scholar]
  • Williams P, Bainton NJ, Swift S, Chhabra SR, Winson MK, Stewart GS, Salmond GP, Bycroft BW. Small molecule-mediated density-dependent control of gene expression in prokaryotes: bioluminescence and the biosynthesis of carbapenem antibiotics. FEMS Microbiol Lett. 1992 Dec 15;100(1-3):161–167. [Abstract] [Google Scholar]
  • Winson MK, Camara M, Latifi A, Foglino M, Chhabra SR, Daykin M, Bally M, Chapon V, Salmond GP, Bycroft BW, et al. Multiple N-acyl-L-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. Proc Natl Acad Sci U S A. 1995 Sep 26;92(20):9427–9431. [Europe PMC free article] [Abstract] [Google Scholar]
  • Yanisch-Perron C, Vieira J, Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. [Abstract] [Google Scholar]
Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

Full text links 

Read article at publisher's site: https://doi.org/10.1128/jb.179.17.5271-5281.1997

Read article for free, from open access legal sources, via Unpaywall: https://europepmc.org/articles/pmc179392?pdf=renderUnpaywall

Free after 4 months at jb.asm.org
http://jb.asm.org/cgi/reprint/179/17/5271

Free to read at jb.asm.org
http://jb.asm.org/cgi/content/abstract/179/17/5271

Citations & impact 

Impact metrics

228
Citations
Jump to Citations
20
Data citations
Jump to Data

Citations of article over time

Alternative metrics

Altmetric item for https://www.altmetric.com/details/13668418
Altmetric
Discover the attention surrounding your research
https://www.altmetric.com/details/13668418

Smart citations by scite.ai
Smart citations by scite.ai include citation statements extracted from the full text of the citing article. The number of the statements may be higher than the number of citations provided by EuropePMC if one paper cites another multiple times or lower if scite has not yet processed some of the citing articles.
Explore citation contexts and check if this article has been supported or disputed.
https://scite.ai/reports/10.1128/jb.179.17.5271-5281.1997

Supporting
Mentioning
Contrasting
14
347
1

Article citations

Go to all (228) article citations

Data 

Data behind the article

This data has been text mined from the article, or deposited into data resources.

BioStudies: supplemental material and supporting data

Similar Articles 

To arrive at the top five similar articles we use a word-weighted algorithm to compare words from the Title and Abstract of each citation.

Funding 

Funders who supported this work.

Wellcome Trust