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 Gallagher, L. A.
Right arrow Articles by Manoil, C.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Gallagher, L. A.
Right arrow Articles by Manoil, C.

 Previous Article  |  Next Article 

Journal of Bacteriology, November 2001, p. 6207-6214, Vol. 183, No. 21
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.21.6207-6214.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Pseudomonas aeruginosa PAO1 Kills Caenorhabditis elegans by Cyanide Poisoning

Larry A. Gallagher and Colin Manoil*

Department of Genetics, University of Washington, Seattle, Washington 98195-7360

Received 4 June 2001/Accepted 2 August 2001

In this report we describe experiments to investigate a simple virulence model in which Pseudomonas aeruginosa PAO1 rapidly paralyzes and kills the nematode Caenorhabditis elegans. Our results imply that hydrogen cyanide is the sole or primary toxic factor produced by P. aeruginosa that is responsible for killing of the nematode. Four lines of evidence support this conclusion. First, a transposon insertion mutation in a gene encoding a subunit of hydrogen cyanide synthase (hcnC) eliminated nematode killing. Second, the 17 avirulent mutants examined all exhibited reduced cyanide synthesis, and the residual production levels correlated with killing efficiency. Third, exposure to exogenous cyanide alone at levels comparable to the level produced by PAO1 killed nematodes with kinetics similar to those observed with bacteria. The killing was not enhanced if hcnC mutant bacteria were present during cyanide exposure. And fourth, a nematode mutant (egl-9) resistant to P. aeruginosa was also resistant to killing by exogenous cyanide in the absence of bacteria. A model for nematode killing based on inhibition of mitochondrial cytochrome oxidase is presented. The action of cyanide helps account for the unusually broad host range of virulence of P. aeruginosa and may contribute to the pathogenesis in opportunistic human infections due to the bacterium.

* Corresponding author. Mailing address: Department of Genetics, University of Washington, Box 357360, Seattle, WA 98195-7360. Phone: (206) 543-7800. Fax: (206) 543-0754. E-mail: manoil{at}u.washington.edu.

Journal of Bacteriology, November 2001, p. 6207-6214, Vol. 183, No. 21
0021-9193/01/$04.00+0   DOI: 10.1128/JB.183.21.6207-6214.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Cody, W. L., Pritchett, C. L., Jones, A. K., Carterson, A. J., Jackson, D., Frisk, A., Wolfgang, M. C., Schurr, M. J. (2009). Pseudomonas aeruginosa AlgR Controls Cyanide Production in an AlgZ-Dependent Manner. J. Bacteriol. 191: 2993-3002 [Abstract] [Full Text]  
  • Farrow, J. M. III, Sund, Z. M., Ellison, M. L., Wade, D. S., Coleman, J. P., Pesci, E. C. (2008). PqsE Functions Independently of PqsR-Pseudomonas Quinolone Signal and Enhances the rhl Quorum-Sensing System. J. Bacteriol. 190: 7043-7051 [Abstract] [Full Text]  
  • Ryall, B., Davies, J. C., Wilson, R., Shoemark, A., Williams, H. D. (2008). Pseudomonas aeruginosa, cyanide accumulation and lung function in CF and non-CF bronchiectasis patients. Eur Respir J 32: 740-747 [Abstract] [Full Text]  
  • Sanderson, K., Wescombe, L., Kirov, S. M., Champion, A., Reid, D. W. (2008). Bacterial cyanogenesis occurs in the cystic fibrosis lung. Eur Respir J 32: 329-333 [Abstract] [Full Text]  
  • Adonizio, A., Leal, S. M. Jr, Ausubel, F. M., Mathee, K. (2008). Attenuation of Pseudomonas aeruginosa virulence by medicinal plants in a Caenorhabditis elegans model system. J Med Microbiol 57: 809-813 [Abstract] [Full Text]  
  • Anderson, G. G., Moreau-Marquis, S., Stanton, B. A., O'Toole, G. A. (2008). In Vitro Analysis of Tobramycin-Treated Pseudomonas aeruginosa Biofilms on Cystic Fibrosis-Derived Airway Epithelial Cells. Infect. Immun. 76: 1423-1433 [Abstract] [Full Text]  
  • Lima, A., Zunino, P., D'Alessandro, B., Piccini, C. (2007). An iron-regulated outer-membrane protein of Proteus mirabilis is a haem receptor that plays an important role in urinary tract infection and in in vivo growth. J Med Microbiol 56: 1600-1607 [Abstract] [Full Text]  
  • Hoogewijs, D., Terwilliger, N. B., Webster, K. A., Powell-Coffman, J. A., Tokishita, S., Yamagata, H., Hankeln, T., Burmester, T., Rytkonen, K. T., Nikinmaa, M., Abele, D., Heise, K., Lucassen, M., Fandrey, J., Maxwell, P. H., Pahlman, S., Gorr, T. A. (2007). From critters to cancers: bridging comparative and clinical research on oxygen sensing, HIF signaling, and adaptations towards hypoxia. Integr. Comp. Biol. 47: 552-577 [Abstract] [Full Text]  
  • Navas, A., Cobas, G., Talavera, M., Ayala, J. A., Lopez, J. A., Martinez, J. L. (2007). Experimental validation of Haldane's hypothesis on the role of infection as an evolutionary force for Metazoans. Proc. Natl. Acad. Sci. USA 104: 13728-13731 [Abstract] [Full Text]  
  • Farrow, J. M. III, Pesci, E. C. (2007). Two Distinct Pathways Supply Anthranilate as a Precursor of the Pseudomonas Quinolone Signal. J. Bacteriol. 189: 3425-3433 [Abstract] [Full Text]  
  • Lujan, A. M., Moyano, A. J., Segura, I., Argarana, C. E., Smania, A. M. (2007). Quorum-sensing-deficient (lasR) mutants emerge at high frequency from a Pseudomonas aeruginosa mutS strain. Microbiology 153: 225-237 [Abstract] [Full Text]  
  • Cipollone, R., Frangipani, E., Tiburzi, F., Imperi, F., Ascenzi, P., Visca, P. (2007). Involvement of Pseudomonas aeruginosa Rhodanese in Protection from Cyanide Toxicity. Appl. Environ. Microbiol. 73: 390-398 [Abstract] [Full Text]  
  • Beale, E., Li, G., Tan, M.-W., Rumbaugh, K. P. (2006). Caenorhabditis elegans Senses Bacterial Autoinducers.. Appl. Environ. Microbiol. 72: 5135-5137 [Abstract] [Full Text]  
  • Xiao, G., He, J., Rahme, L. G. (2006). Mutation analysis of the Pseudomonas aeruginosa mvfR and pqsABCDE gene promoters demonstrates complex quorum-sensing circuitry. Microbiology 152: 1679-1686 [Abstract] [Full Text]  
  • Zlosnik, J. E. A., Tavankar, G. R., Bundy, J. G., Mossialos, D., O'Toole, R., Williams, H. D. (2006). Investigation of the physiological relationship between the cyanide-insensitive oxidase and cyanide production in Pseudomonas aeruginosa.. Microbiology 152: 1407-1415 [Abstract] [Full Text]  
  • An, D., Danhorn, T., Fuqua, C., Parsek, M. R. (2006). Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures.. Proc. Natl. Acad. Sci. USA 103: 3828-3833 [Abstract] [Full Text]  
  • Furukawa, S., Kuchma, S. L., O'Toole, G. A. (2006). Keeping Their Options Open: Acute versus Persistent Infections. J. Bacteriol. 188: 1211-1217 [Full Text]  
  • Anjum, M. F., Marooney, C., Fookes, M., Baker, S., Dougan, G., Ivens, A., Woodward, M. J. (2005). Identification of Core and Variable Components of the Salmonella enterica Subspecies I Genome by Microarray. Infect. Immun. 73: 7894-7905 [Abstract] [Full Text]  
  • Palmer, K. L., Mashburn, L. M., Singh, P. K., Whiteley, M. (2005). Cystic Fibrosis Sputum Supports Growth and Cues Key Aspects of Pseudomonas aeruginosa Physiology. J. Bacteriol. 187: 5267-5277 [Abstract] [Full Text]  
  • Baysse, C., Cullinane, M., Denervaud, V., Burrowes, E., Dow, J. M., Morrissey, J. P., Tam, L., Trevors, J. T., O'Gara, F. (2005). Modulation of quorum sensing in Pseudomonas aeruginosa through alteration of membrane properties. Microbiology 151: 2529-2542 [Abstract] [Full Text]  
  • Mylonakis, E., Aballay, A. (2005). Worms and Flies as Genetically Tractable Animal Models To Study Host-Pathogen Interactions. Infect. Immun. 73: 3833-3841 [Full Text]  
  • Aendekerk, S., Diggle, S. P., Song, Z., Hoiby, N., Cornelis, P., Williams, P., Camara, M. (2005). The MexGHI-OpmD multidrug efflux pump controls growth, antibiotic susceptibility and virulence in Pseudomonas aeruginosa via 4-quinolone-dependent cell-to-cell communication. Microbiology 151: 1113-1125 [Abstract] [Full Text]  
  • Rasmussen, T. B., Bjarnsholt, T., Skindersoe, M. E., Hentzer, M., Kristoffersen, P., Kote, M., Nielsen, J., Eberl, L., Givskov, M. (2005). Screening for Quorum-Sensing Inhibitors (QSI) by Use of a Novel Genetic System, the QSI Selector. J. Bacteriol. 187: 1799-1814 [Abstract] [Full Text]  
  • Kuchma, S. L., Connolly, J. P., O'Toole, G. A. (2005). A Three-Component Regulatory System Regulates Biofilm Maturation and Type III Secretion in Pseudomonas aeruginosa. J. Bacteriol. 187: 1441-1454 [Abstract] [Full Text]  
  • Luque-Almagro, V. M., Huertas, M.-J., Martinez-Luque, M., Moreno-Vivian, C., Roldan, M. D., Garcia-Gil, L. J., Castillo, F., Blasco, R. (2005). Bacterial Degradation of Cyanide and Its Metal Complexes under Alkaline Conditions. Appl. Environ. Microbiol. 71: 940-947 [Abstract] [Full Text]  
  • Calfee, M. W., Shelton, J. G., McCubrey, J. A., Pesci, E. C. (2005). Solubility and Bioactivity of the Pseudomonas Quinolone Signal Are Increased by a Pseudomonas aeruginosa-Produced Surfactant. Infect. Immun. 73: 878-882 [Abstract] [Full Text]  
  • Carterson, A. J., Morici, L. A., Jackson, D. W., Frisk, A., Lizewski, S. E., Jupiter, R., Simpson, K., Kunz, D. A., Davis, S. H., Schurr, J. R., Hassett, D. J., Schurr, M. J. (2004). The Transcriptional Regulator AlgR Controls Cyanide Production in Pseudomonas aeruginosa. J. Bacteriol. 186: 6837-6844 [Abstract] [Full Text]  
  • Lizewski, S. E., Schurr, J. R., Jackson, D. W., Frisk, A., Carterson, A. J., Schurr, M. J. (2004). Identification of AlgR-Regulated Genes in Pseudomonas aeruginosa by Use of Microarray Analysis. J. Bacteriol. 186: 5672-5684 [Abstract] [Full Text]  
  • Moy, T. I., Mylonakis, E., Calderwood, S. B., Ausubel, F. M. (2004). Cytotoxicity of Hydrogen Peroxide Produced by Enterococcus faecium. Infect. Immun. 72: 4512-4520 [Abstract] [Full Text]  
  • D'Argenio, D. A., Miller, S. I. (2004). Cyclic di-GMP as a bacterial second messenger. Microbiology 150: 2497-2502 [Abstract] [Full Text]  
  • Treinin, M., Shliar, J., Jiang, H., Powell-Coffman, J. A., Bromberg, Z., Horowitz, M. (2003). HIF-1 is required for heat acclimation in the nematode Caenorhabditis elegans. Physiol. Genomics 14: 17-24 [Abstract] [Full Text]  
  • Cooper, M., Tavankar, G. R., Williams, H. D. (2003). Regulation of expression of the cyanide-insensitive terminal oxidase in Pseudomonas aeruginosa. Microbiology 149: 1275-1284 [Abstract] [Full Text]  
  • Tavankar, G. R., Mossialos, D., Williams, H. D. (2003). Mutation or Overexpression of a Terminal Oxidase Leads to a Cell Division Defect and Multiple Antibiotic Sensitivity in Pseudomonas aeruginosa. J. Biol. Chem. 278: 4524-4530 [Abstract] [Full Text]  
  • Firoved, A. M., Deretic, V. (2003). Microarray Analysis of Global Gene Expression in Mucoid Pseudomonas aeruginosa. J. Bacteriol. 185: 1071-1081 [Abstract] [Full Text]  
  • Gallagher, L. A., McKnight, S. L., Kuznetsova, M. S., Pesci, E. C., Manoil, C. (2002). Functions Required for Extracellular Quinolone Signaling by Pseudomonas aeruginosa. J. Bacteriol. 184: 6472-6480 [Abstract] [Full Text]  
  • D'Argenio, D. A., Calfee, M. W., Rainey, P. B., Pesci, E. C. (2002). Autolysis and Autoaggregation in Pseudomonas aeruginosa Colony Morphology Mutants. J. Bacteriol. 184: 6481-6489 [Abstract] [Full Text]  
  • Lizewski, S. E., Lundberg, D. S., Schurr, M. J. (2002). The Transcriptional Regulator AlgR Is Essential for Pseudomonas aeruginosa Pathogenesis. Infect. Immun. 70: 6083-6093 [Abstract] [Full Text]  
  • Reimmann, C., Ginet, N., Michel, L., Keel, C., Michaux, P., Krishnapillai, V., Zala, M., Heurlier, K., Triandafillu, K., Harms, H., Defago, G., Haas, D. (2002). Genetically programmed autoinducer destruction reduces virulence gene expression and swarming motility in Pseudomonas aeruginosa PAO1. Microbiology 148: 923-932 [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»