Journal of Chemical Ecology

, Volume 32, Issue 8, pp 1769–1778 | Cite as

Structural Elucidation and Biological Activity of Acyl-homoserine Lactones from the Phytopathogen Pantoea ananatis Serrano 1928

  • Armando M. Pomini
  • Welington L. Araújo
  • Anita J. Marsaioli
Article

Abstract

In Gram-negative bacteria, the acyl-homoserine lactones (acyl-HSLs) are the main signaling substances employed in cell-to-cell communication systems. This paper describes the chemical characterization of acyl-HSLs produced by the worldwide-spread phytopathogen Pantoea ananatis (Serrano 1928) by using gas chromatography-electron impact mass spectrometry. The absolute configuration of the major identified substance, (S)-(−)-N-hexanoyl-HSL, was determined with gas chromatography-flame ionization detection with a chiral capillary column. Biological activities of extracts, fractions, and synthetic products were evaluated with the specific reporter Agrobacterium tumefaciensNTL4(pZLR4) in β-galactosidase expression assays.

Keywords

Pantoea ananatis Acyl-homoserine lactones Absolute configuration Quorum-sensing Agrobacterium tumefaciens reporter assay 

Notes

Acknowledgments

The authors are indebted to FAPESP for financial support and for a scholarship awarded to A. M. Pomini (process n. 03/09357-7). We wish to express our gratitude to Carol H. Collins (IQ/Unicamp) for revising the manuscript.

References

  1. Azad, H. R., Holmes, G. J., and Cooksey, D. A. 2000. A new leaf blotch disease of sudangrass caused by Pantoea ananas and Pantoea stewartii. Plant Dis. 84:973–979.CrossRefGoogle Scholar
  2. Bainton, N. J., Stead, P., Chhabra, S. R., Bycroft, B. W., Salmond, G. P., Stewart, G. S., and Williams, P. 1992. N-(3-Oxohexanoyl)-l-homoserine lactone regulates carbapenem antibiotic production in Erwinia carotovora. Biochem. J. 288:997–1004.PubMedGoogle Scholar
  3. Blosser, R. S. and Gray, K. M. 2000. Extraction of violacein from Chromobacterium violaceum provides a new quantitative bioassay for N-acyl homoserine lactone autoinducers. J. Microbiol. Methods. 40:47–55.PubMedCrossRefGoogle Scholar
  4. Bodman, S. B. V. and Farrand, S. K. 1995. Capsular polysaccharide biosynthesis and pathogenicity in Erwinia stewartii require induction by an N-acylhomoserine lactone autoinducer. J. Bacteriol. 177:5000–5008.Google Scholar
  5. Cha, C., Gao, P., Chen, Y-C., Shaw, P. D., and Farrand, S. K. 1998. Production of acyl-homoserine lactone quorum-sensing signals by Gram-negative plant-associated bacteria. Mol. Plant–Microbe Interact. 11:1119–1129.PubMedCrossRefGoogle Scholar
  6. Chhabra, S. R., Stead, P., Bainton, N. J., Salmond, G. P. C., Stewart, G. S. A. B., Williams, P., and Bycroft, B. W. 1993. Autoregulation of carbapenem biosynthesis in Erwinia carotovora by analogs of N-(3-oxohexanoyl)- l-homoserine lactone. J. Antibiot. 46:441–454.PubMedGoogle Scholar
  7. Cother, E. J., Reinke, R., McKenzie, C., Lanoiselet, V. M., and Noble, D. H. 2004. An unusual stem necrosis of rice caused by Pantoea ananas and the first record of this pathogen on rice in Australia. Australas. Plant Pathol. 33:495–503.CrossRefGoogle Scholar
  8. Coutinho, T. A., Preisig, O., Mergaert, J., Cnockaert, M. C., Riedel, K.-H., Swings, J., and Wingfield, M. J. 2002. Bacterial blight and dieback of eucalyptus species, hybrids, and clones in South Africa. Plant Dis. 86:20–25.CrossRefGoogle Scholar
  9. Eberhard, A., Burlingame, A. L., Eberhard, C., Kenyon, G. L., Nealson, K. H., and Oppenhemer, N. J. 1981. Structural identification of autoinducer of Photobacterium fischeri luciferase. Biochemistry 20:2444–2449.PubMedCrossRefGoogle Scholar
  10. Engebrecht, J. and Silverman, M. 1984. Identification of genes and gene products necessary for bacterial bioluminescence. Proc. Natl. Acad. Sci. USA 81:4154–4158.PubMedCrossRefGoogle Scholar
  11. Fuqua, C. and Greenberg, E. P. 1998. Self perception in bacteria: quorum sensing with acylated homoserine lactones. Curr. Opin. Microbiol. 1:183–189.PubMedCrossRefGoogle Scholar
  12. Hauben, L., Moore, E. R., Vauterin, L., Steenackers, M., Mergaert, J., Verdonck, L., and Swings, J. 1998. Phylogenetic position of phytopathogens within the Enterobacteriaceae. Syst. Appl. Microbiol. 21:384–397.PubMedGoogle Scholar
  13. Horng, Y. T., Deng, S. C., Daykin, M., Soo, P. C., Wei, J. R., Luh, K. T., Ho, S. W., Swift, S., Lai, H. C., and Williams, P. 2002. The LuxR family protein SpnR functions as a negative regulator of N-acylhomoserine lactone-dependent quorum sensing in Serratia marcescens. Mol. Microbiol. 45:1655–1671.PubMedCrossRefGoogle Scholar
  14. Jones, S., Yu, B., Bainton, N. J., Birdsall, M., Bycroft, B. W., Chhabra, S. R., Cox, A. J. R., Golby, P., Reeves, P. J., Stephens, S., Winson, M. K., Salmond, G. P. C., Stewart, G. S. A. B., and Williams, P. 1993. The lux autoinducer regulates the production of exoenzyme virulence determinants in Erwinia carotovora and Pseudomonas aeruginosa. EMBO J. 12:2477–2482.PubMedGoogle Scholar
  15. Lao, W., Kjelleberg, S., Kumar, N., Denys, R., Read, R. W., and Steinberg, P. 1999. 13C NMR study of N-acyl-S-homoserine lactone derivatives. Magn. Reson. Chem. 37:157–158.CrossRefGoogle Scholar
  16. Lithgow, J. K., Wilkinson, A., Hardman, A., Rodelas, B., Wisniewski-D, F., Williams, P., and Downie, J. A. 2000. The regulatory locus cinRI in Rhizobium leguminosarum controls a network of quorum-sensing loci. Mol. Microbiol. 37:81–97.PubMedCrossRefGoogle Scholar
  17. Marketon, M. M., Gronquist, M. R., Eberhard, A., and González, J. E. 2002. Characterization of the Sinorhizobium meliloti sinR/sinI locus and the production of novel N-acyl homoserine lactones. J. Bacteriol. 184:5686–5695.PubMedCrossRefGoogle Scholar
  18. Morohoshi, T., Inaba, T., Kato, N., Kanai, K., and Ikeda, T. 2004. Identification of quorum-sensing signal molecules and the LuxRI homologues in the fish pathogen Edwardsiella tarda. J. Biosci. Bioeng. 98:274–281.PubMedGoogle Scholar
  19. Paccola-Meirelles, L. D., Ferreira, A. S., Meirelles, W. F., Marriel, I. E., and Casela, C. R. 2001. Detection of a bacterium associated with a leaf spot disease of maize in Brazil. J. Phytopathol. 149:275–279.CrossRefGoogle Scholar
  20. Pearson, J. P., Gray, K. M., Passador, L., Tucker, K. D., Eberhard, A., Iglewski, B. H., and Greenberg, E. P. 1994. Structure of the autoinducer required for expression of Pseudomonas aeruginosa virulence genes. Proc. Natl. Acad. Sci. USA 91:197–201.PubMedCrossRefGoogle Scholar
  21. Piper, K. R., Bodman, S. B. V., and Farrand, S. K. 1993. Conjugation factor of Agrobacterium tumefaciens regulates Ti plasmid transfer by autoinduction. Nature 362:448–450.PubMedCrossRefGoogle Scholar
  22. Pomini, A. M., Araújo, W. L., Manfio, G. P., and Marsaioli, A. J. 2005. Acyl-homoserine lactones from Erwinia psidii R. IBSBF 435T, a guava phytopathogen (Psidium guajava L.). J. Agric. Food Chem. 53:6262–6265.PubMedCrossRefGoogle Scholar
  23. Ravn, L., Christensen, A. B., Molin, S., Givskov, M. and Gram, L. 2001. Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. J. Microbiol. Methods 44:239–251.PubMedCrossRefGoogle Scholar
  24. Roche, D. M., Byers, J. T., Smith, D. S., Glansdorp, F. G., Spring, D. R., and Welch, M. 2004. Communications blackout? Do N-acylhomoserine lactone-degrading enzymes have any role in quorum sensing? Microbiology 150:2023–2028.PubMedCrossRefGoogle Scholar
  25. Schaefer, A. L., Val, D. L., Hamzelka, B. L., Cronan, J. E., and Greenberg, E. P. 1996. 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. USA 93:9505–9509.PubMedCrossRefGoogle Scholar
  26. Serrano, F. B. 1928. Bacterial fruitlet brown-rot of pineapple in the Philippines. Philipp. J. Sci. 36:271–305.Google Scholar
  27. Suga, H. and Smith, K. M. 2003. Molecular mechanisms of bacterial quorum-sensing as a new drug target. Curr. Opin. Chem. Biol. 7:586–591.PubMedCrossRefGoogle Scholar
  28. Venturi, V., Venuti, C., Devescovi, G., Lucchese, C., Friscina, A., Degrassi, G., Aguilar, C., and Mazzucchi, U. 2004. The plant pathogen Erwinia amylovora produces acyl-homoserine lactone signal molecules in vitro and in planta. FEMS Microbiol. Lett. 241:179–183.PubMedCrossRefGoogle Scholar
  29. Walcott, R. R., Gitaitis, R. D., Castro, A. C., Sanders, F. H. Jr., and Diaz-Perez, J. C. 2002. Natural infestation of onion seed by Pantoea ananatis, causal agent of center rot. Plant Dis. 86:106–111.CrossRefGoogle Scholar
  30. Whitehead, N. A., Barnard, A. M., Slater, H., Simpson, N. J. L., and Salmond, G. P. C. 2001. Quorum-sensing in Gram-negative bacteria. FEMS Microbiol. Rev. 25:365–404.PubMedCrossRefGoogle Scholar
  31. Whithers, H., Swift, S., and Williams, P. 2001. Quorum sensing as an integral component of gene regulatory networks in Gram-negative bacteria. Curr. Opin. Microbiol. 4:186–193.CrossRefGoogle Scholar
  32. Zhang, L., Murphy, P. J., Kerr, A. and Tate, M. E. 1993. Agrobacterium conjugation and gene regulation by N-acyl- l-homoserine lactones. Nature 362:446–448.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2006

Authors and Affiliations

  • Armando M. Pomini
    • 1
  • Welington L. Araújo
    • 2
  • Anita J. Marsaioli
    • 1
  1. 1.Chemistry InstituteState University of CampinasCampinas,SPBrazil
  2. 2.Genetic Department, ESALQState University of São PauloPiracicaba,SPBrazil

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