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 Schreiber, K.
Right arrow Articles by Schobert, M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Schreiber, K.
Right arrow Articles by Schobert, M.

 Previous Article  |  Next Article 

Journal of Bacteriology, January 2006, p. 659-668, Vol. 188, No. 2
0021-9193/06/$08.00+0     doi:10.1128/JB.188.2.659-668.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.

Anaerobic Survival of Pseudomonas aeruginosa by Pyruvate Fermentation Requires an Usp-Type Stress Protein

Kerstin Schreiber,1 Nelli Boes,1 Martin Eschbach,1 Lothar Jaensch,2 Juergen Wehland,2 Thomas Bjarnsholt,3 Michael Givskov,3 Morten Hentzer,3,{dagger} and Max Schobert1*

Institute of Microbiology, Technical University Braunschweig, Spielmannstr. 7, D-38106 Braunschweig, Germany,1 Department of Cell Biology, German Research Centre for Biotechnology, Mascheroder Weg 1, D-38124 Braunschweig, Germany,2 Center for Biomedical Microbiology, BioCentrum-DTU, Technical University of Denmark, DK-2800 Kgs. Lyngby, Denmark3

Received 1 July 2005/ Accepted 13 October 2005

Recently, we identified a pyruvate fermentation pathway in Pseudomonas aeruginosa sustaining anaerobic survival in the absence of alternative anaerobic respiratory and fermentative energy generation systems (M. Eschbach, K. Schreiber, K. Trunk, J. Buer, D. Jahn, and M. Schobert, J. Bacteriol. 186:4596-4604, 2004). Anaerobic long-term survival of P. aeruginosa might be essential for survival in deeper layers of a biofilm and the persistent infection of anaerobic mucus plaques in the cystic fibrosis lung. Proteome analysis of P. aeruginosa cells during a 7-day period of pyruvate fermentation revealed the induced synthesis of three enzymes involved in arginine fermentation, ArcA, ArcB, and ArcC, and the outer membrane protein OprL. Moreover, formation of two proteins of unknown function, PA3309 and PA4352, increased by factors of 72- and 22-fold, respectively. Both belong to the group of universal stress proteins (Usp). Long-term survival of a PA3309 knockout mutant by pyruvate fermentation was found drastically reduced. The oxygen-sensing regulator Anr controls expression of the PPA3309-lacZ reporter gene fusion after a shift to anaerobic conditions and further pyruvate fermentation. PA3309 expression was also found induced during the anaerobic and aerobic stationary phases. This aerobic stationary-phase induction is independent of the regulatory proteins Anr, RpoS, RelA, GacA, RhlR, and LasR, indicating a currently unknown mechanism of stationary-phase-dependent gene activation. PA3309 promoter activity was detected in the deeper layers of a P. aeruginosa biofilm using a PPA3309-gfp (green fluorescent protein gene) fusion and confocal laser-scanning microscopy. This is the first description of an Anr-dependent, anaerobically induced, and functional Usp-like protein in bacteria.

* Corresponding author: Mailing address: Institute of Microbiology, Technical University Braunschweig, Spielmannstr. 7, D-38106 Braunschweig, Germany. Phone: 49 531 3915857. Fax: 49 531 3915854.E-mail: m.schobert{at}tu-bs.de.

{dagger} Present address: Carlsberg Research Center, Biosector, Gamle Carlsberg Vej 10, DK-2500 Valby, Denmark.

Journal of Bacteriology, January 2006, p. 659-668, Vol. 188, No. 2
0021-9193/06/$08.00+0     doi:10.1128/JB.188.2.659-668.2006
Copyright © 2006, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Van Alst, N. E., Wellington, M., Clark, V. L., Haidaris, C. G., Iglewski, B. H. (2009). Nitrite Reductase NirS Is Required for Type III Secretion System Expression and Virulence in the Human Monocyte Cell Line THP-1 by Pseudomonas aeruginosa. Infect. Immun. 77: 4446-4454 [Abstract] [Full Text]  
  • Mikkelsen, H., Bond, N. J., Skindersoe, M. E., Givskov, M., Lilley, K. S., Welch, M. (2009). Biofilms and type III secretion are not mutually exclusive in Pseudomonas aeruginosa. Microbiology 155: 687-698 [Abstract] [Full Text]  
  • Boes, N., Schreiber, K., Schobert, M. (2008). SpoT-Triggered Stringent Response Controls usp Gene Expression in Pseudomonas aeruginosa. J. Bacteriol. 190: 7189-7199 [Abstract] [Full Text]  
  • Benkert, B., Quack, N., Schreiber, K., Jaensch, L., Jahn, D., Schobert, M. (2008). Nitrate-responsive NarX-NarL represses arginine-mediated induction of the Pseudomonas aeruginosa arginine fermentation arcDABC operon. Microbiology 154: 3053-3060 [Abstract] [Full Text]  
  • Panmanee, W., Gomez, F., Witte, D., Pancholi, V., Britigan, B. E., Hassett, D. J. (2008). The Peptidoglycan-Associated Lipoprotein OprL Helps Protect a Pseudomonas aeruginosa Mutant Devoid of the Transactivator OxyR from Hydrogen Peroxide-Mediated Killing during Planktonic and Biofilm Culture. J. Bacteriol. 190: 3658-3669 [Abstract] [Full Text]  
  • Goldberg, J. B., Hancock, R. E. W., Parales, R. E., Loper, J., Cornelis, P. (2008). Pseudomonas 2007. J. Bacteriol. 190: 2649-2662 [Full Text]  
  • Arai, H., Roh, J. H., Kaplan, S. (2008). Transcriptome Dynamics during the Transition from Anaerobic Photosynthesis to Aerobic Respiration in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 190: 286-299 [Abstract] [Full Text]  
  • Price-Whelan, A., Dietrich, L. E. P., Newman, D. K. (2007). Pyocyanin Alters Redox Homeostasis and Carbon Flux through Central Metabolic Pathways in Pseudomonas aeruginosa PA14. J. Bacteriol. 189: 6372-6381 [Abstract] [Full Text]  
  • Mikkelsen, H., Duck, Z., Lilley, K. S., Welch, M. (2007). Interrelationships between Colonies, Biofilms, and Planktonic Cells of Pseudomonas aeruginosa. J. Bacteriol. 189: 2411-2416 [Abstract] [Full Text]  
  • Meshulam-Simon, G., Behrens, S., Choo, A. D., Spormann, A. M. (2007). Hydrogen Metabolism in Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 73: 1153-1165 [Abstract] [Full Text]  
  • Choi, C., Munch, R., Leupold, S., Klein, J., Siegel, I., Thielen, B., Benkert, B., Kucklick, M., Schobert, M., Barthelmes, J., Ebeling, C., Haddad, I., Scheer, M., Grote, A., Hiller, K., Bunk, B., Schreiber, K., Retter, I., Schomburg, D., Jahn, D. (2007). SYSTOMONAS -- an integrated database for systems biology analysis of Pseudomonas. Nucleic Acids Res 35: D533-D537 [Abstract] [Full Text]  
  • Boes, N., Schreiber, K., Hartig, E., Jaensch, L., Schobert, M. (2006). The Pseudomonas aeruginosa Universal Stress Protein PA4352 Is Essential for Surviving Anaerobic Energy Stress.. J. Bacteriol. 188: 6529-6538 [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»