This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Huang, J. J.
Right arrow Articles by Leadbetter, J. R.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Huang, J. J.
Right arrow Articles by Leadbetter, J. R.
Agricola
Right arrow Articles by Huang, J. J.
Right arrow Articles by Leadbetter, J. R.

 Previous Article  |  Next Article 

Applied and Environmental Microbiology, October 2003, p. 5941-5949, Vol. 69, No. 10
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.10.5941-5949.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Utilization of Acyl-Homoserine Lactone Quorum Signals for Growth by a Soil Pseudomonad and Pseudomonas aeruginosa PAO1

Jean J. Huang,1 Jong-In Han,2 Lian-Hui Zhang,3,4 and Jared R. Leadbetter2*

Departments of Biology,1 Environmental Science and Engineering, W. M. Keck Laboratories, California Institute of Technology, Pasadena, California 91125,2 Institute of Molecular and Cell Biology, Singapore 117609,3 Department of Biological Sciences, The National University of Singapore, Singapore 119260, Republic of Singapore4

Received 15 May 2003/ Accepted 17 July 2003

Acyl-homoserine lactones (AHLs) are employed by several Proteobacteria as quorum-sensing signals. Past studies have established that these compounds are subject to biochemical decay and can be used as growth nutrients. Here we describe the isolation of a soil bacterium, Pseudomonas strain PAI-A, that degrades 3-oxododecanoyl-homoserine lactone (3OC12HSL) and other long-acyl, but not short-acyl, AHLs as sole energy sources for growth. The small-subunit rRNA gene from strain PAI-A was 98.4% identical to that of Pseudomonas aeruginosa, but the soil isolate did not produce obvious pigments or AHLs or grow under denitrifying conditions or at 42°C. The quorum-sensing bacterium P. aeruginosa, which produces both 3OC12HSL and C4HSL, was examined for the ability to utilize AHLs for growth. It did so with a specificity similar to that of strain PAI-A, i.e., degrading long-acyl but not short-acyl AHLs. In contrast to the growth observed with strain PAI-A, P. aeruginosa strain PAO1 growth on AHLs commenced only after extremely long lag phases. Liquid-chromatography-atmospheric pressure chemical ionization-mass spectrometry analyses indicate that strain PAO1 degrades long-acyl AHLs via an AHL acylase and a homoserine-generating HSL lactonase. A P. aeruginosa gene, pvdQ (PA2385), has previously been identified as being a homologue of the AHL acylase described as occurring in a Ralstonia species. Escherichia coli expressing pvdQ catalyzed the rapid inactivation of long-acyl AHLs and the release of HSL. P. aeruginosa engineered to constitutively express pvdQ did not accumulate its 3OC12HSL quorum signal when grown in rich media. However, pvdQ knockout mutants of P. aeruginosa were still able to grow by utilizing 3OC12HSL. To our knowledge, this is the first report of the degradation of AHLs by pseudomonads or other {gamma}-Proteobacteria, of AHL acylase activity in a quorum-sensing bacterium, of HSL lactonase activity in any bacterium, and of AHL degradation with specificity only towards AHLs with long side chains.

* Corresponding author. Mailing address: Environmental Science & Engineering, W. M. Keck Laboratories, M/C 138-78, California Institute of Technology, Pasadena, CA 91125. Phone: (626) 395-4182. Fax: (626) 395-2940. E-mail: jleadbetter{at}caltech.edu.

Applied and Environmental Microbiology, October 2003, p. 5941-5949, Vol. 69, No. 10
0099-2240/03/$08.00+0     DOI: 10.1128/AEM.69.10.5941-5949.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Gan, H. M., Buckley, L., Szegedi, E., Hudson, A. O., Savka, M. A. (2009). Identification of an rsh Gene from a Novosphingobium sp. Necessary for Quorum-Sensing Signal Accumulation. J. Bacteriol. 191: 2551-2560 [Abstract] [Full Text]  
  • Shepherd, R. W., Lindow, S. E. (2009). Two Dissimilar N-Acyl-Homoserine Lactone Acylases of Pseudomonas syringae Influence Colony and Biofilm Morphology. Appl. Environ. Microbiol. 75: 45-53 [Abstract] [Full Text]  
  • Schipper, C., Hornung, C., Bijtenhoorn, P., Quitschau, M., Grond, S., Streit, W. R. (2009). Metagenome-Derived Clones Encoding Two Novel Lactonase Family Proteins Involved in Biofilm Inhibition in Pseudomonas aeruginosa. Appl. Environ. Microbiol. 75: 224-233 [Abstract] [Full Text]  
  • Overhage, J., Bains, M., Brazas, M. D., Hancock, R. E. W. (2008). Swarming of Pseudomonas aeruginosa Is a Complex Adaptation Leading to Increased Production of Virulence Factors and Antibiotic Resistance. J. Bacteriol. 190: 2671-2679 [Abstract] [Full Text]  
  • Uroz, S., Oger, P. M., Chapelle, E., Adeline, M.-T., Faure, D., Dessaux, Y. (2008). A Rhodococcus qsdA-Encoded Enzyme Defines a Novel Class of Large-Spectrum Quorum-Quenching Lactonases. Appl. Environ. Microbiol. 74: 1357-1366 [Abstract] [Full Text]  
  • Dong, Y.-H., Wang, L.-H., Zhang, L.-H. (2007). Quorum-quenching microbial infections: mechanisms and implications. Phil Trans R Soc B 362: 1201-1211 [Abstract] [Full Text]  
  • Bjarnsholt, T., Givskov, M. (2007). Quorum-sensing blockade as a strategy for enhancing host defences against bacterial pathogens. Phil Trans R Soc B 362: 1213-1222 [Abstract] [Full Text]  
  • Manefield, M., Whiteley, A. S (2007). Acylated homoserine lactones in the environment: chameleons of bioactivity. Phil Trans R Soc B 362: 1235-1240 [Abstract] [Full Text]  
  • Duan, K., Surette, M. G. (2007). Environmental Regulation of Pseudomonas aeruginosa PAO1 Las and Rhl Quorum-Sensing Systems. J. Bacteriol. 189: 4827-4836 [Abstract] [Full Text]  
  • DeAngelis, K. M., Firestone, M. K., Lindow, S. E. (2007). Sensitive Whole-Cell Biosensor Suitable for Detecting a Variety of N-Acyl Homoserine Lactones in Intact Rhizosphere Microbial Communities. Appl. Environ. Microbiol. 73: 3724-3727 [Abstract] [Full Text]  
  • Gonzalez, J. E., Keshavan, N. D. (2006). Messing with Bacterial Quorum Sensing. Microbiol. Mol. Biol. Rev. 70: 859-875 [Abstract] [Full Text]  
  • Koutsoudis, M. D., Tsaltas, D., Minogue, T. D., von Bodman, S. B. (2006). Quorum-sensing regulation governs bacterial adhesion, biofilm development, and host colonization in Pantoea stewartii subspecies stewartii. Proc. Natl. Acad. Sci. USA 103: 5983-5988 [Abstract] [Full Text]  
  • Rasmussen, T. B., Givskov, M. (2006). Quorum sensing inhibitors: a bargain of effects.. Microbiology 152: 895-904 [Abstract] [Full Text]  
  • Sio, C. F., Otten, L. G., Cool, R. H., Diggle, S. P., Braun, P. G., Bos, R., Daykin, M., Camara, M., Williams, P., Quax, W. J. (2006). Quorum Quenching by an N-Acyl-Homoserine Lactone Acylase from Pseudomonas aeruginosa PAO1. Infect. Immun. 74: 1673-1682 [Abstract] [Full Text]  
  • Huang, J. J., Petersen, A., Whiteley, M., Leadbetter, J. R. (2006). Identification of QuiP, the Product of Gene PA1032, as the Second Acyl-Homoserine Lactone Acylase of Pseudomonas aeruginosa PAO1. Appl. Environ. Microbiol. 72: 1190-1197 [Abstract] [Full Text]  
  • Uroz, S., Chhabra, S. R., Camara, M., Williams, P., Oger, P., Dessaux, Y. (2005). N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151: 3313-3322 [Abstract] [Full Text]  
  • Park, S.-Y., Kang, H.-O., Jang, H.-S., Lee, J.-K., Koo, B.-T., Yum, D.-Y. (2005). Identification of Extracellular N-Acylhomoserine Lactone Acylase from a Streptomyces sp. and Its Application to Quorum Quenching. Appl. Environ. Microbiol. 71: 2632-2641 [Abstract] [Full Text]  
  • Wang, Y.-J., Leadbetter, J. R. (2005). Rapid Acyl-Homoserine Lactone Quorum Signal Biodegradation in Diverse Soils. Appl. Environ. Microbiol. 71: 1291-1299 [Abstract] [Full Text]  
  • Ulrich, R. L. (2004). Quorum Quenching: Enzymatic Disruption of N-Acylhomoserine Lactone-Mediated Bacterial Communication in Burkholderia thailandensis. Appl. Environ. Microbiol. 70: 6173-6180 [Abstract] [Full Text]  
  • Roche, D. M., Byers, J. T., Smith, D. S., Glansdorp, F. G., Spring, D. R., Welch, M. (2004). Communications blackout? Do N-acylhomoserine-lactone-degrading enzymes have any role in quorum sensing?. Microbiology 150: 2023-2028 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»