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Nitric oxide signaling in pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic Di-GMP levels, and enhanced dispersal

Nitric oxide signaling in pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic Di-GMP levels, and enhanced dispersal
Nitric oxide signaling in pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic Di-GMP levels, and enhanced dispersal
Bacteria in biofilms often undergo active dispersal events and revert to a free-swimming, planktonic state to complete the biofilm life cycle. The signaling molecule nitric oxide (NO) was previously found to trigger biofilm dispersal in the opportunistic pathogen Pseudomonas aeruginosa at low, nontoxic concentrations (N. Barraud, D. J. Hassett, S. H. Hwang, S. A. Rice, S. Kjelleberg, and J. S. Webb, J. Bacteriol. 188:7344-7353, 2006).

NO was further shown to increase cell motility and susceptibility to antimicrobials. Recently, numerous studies revealed that increased degradation of the secondary messenger cyclic di-GMP (c-di-GMP) by specific phosphodiesterases (PDEs) triggers a planktonic mode of growth in eubacteria. In this study, the potential link between NO and c-di-GMP signaling was investigated by performing (i) PDE inhibitor studies, (ii) enzymatic assays to measure PDE activity, and (iii) direct quantification of intracellular c-di-GMP levels.

The results suggest a role for c-di-GMP signaling in triggering the biofilm dispersal event induced by NO, as dispersal requires PDE activity and addition of NO stimulates PDE and induces the concomitant decrease in intracellular c-di-GMP levels in P. aeruginosa. Furthermore, gene expression studies indicated global responses to low, nontoxic levels of NO in P. aeruginosa biofilms, including upregulation of genes involved in motility and energy metabolism and downregulation of adhesins and virulence factors.

Finally, site-directed mutagenesis of candidate genes and physiological characterization of the corresponding mutant strains uncovered that the chemotaxis transducer BdlA is involved in the biofilm dispersal response induced by NO.
0021-9193
7333-7342
Barraud, Nicholas
4866af39-44cf-432d-9232-b0dac43f8ac3
Schleheck, David
bec76f0f-ff08-471b-953f-50ca0ddc9e91
Klebensberger, Janosch
41a6a6f1-643f-4513-8614-f3d82a919310
Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Hassett, Daniel J.
5d8fe550-d498-4b3d-beba-f11519251681
Rice, Scott A.
4f9516db-1d35-4211-878c-bb6cfb2a6b4a
Kjelleberg, Staffan
043b66b5-130c-42f2-99b3-ec3eecf3248e
Barraud, Nicholas
4866af39-44cf-432d-9232-b0dac43f8ac3
Schleheck, David
bec76f0f-ff08-471b-953f-50ca0ddc9e91
Klebensberger, Janosch
41a6a6f1-643f-4513-8614-f3d82a919310
Webb, Jeremy S.
ec0a5c4e-86cc-4ae9-b390-7298f5d65f8d
Hassett, Daniel J.
5d8fe550-d498-4b3d-beba-f11519251681
Rice, Scott A.
4f9516db-1d35-4211-878c-bb6cfb2a6b4a
Kjelleberg, Staffan
043b66b5-130c-42f2-99b3-ec3eecf3248e

Barraud, Nicholas, Schleheck, David, Klebensberger, Janosch, Webb, Jeremy S., Hassett, Daniel J., Rice, Scott A. and Kjelleberg, Staffan (2009) Nitric oxide signaling in pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic Di-GMP levels, and enhanced dispersal. Journal of Bacteriology, 191 (23), 7333-7342. (doi:10.1128/JB.00975-09).

Record type: Article

Abstract

Bacteria in biofilms often undergo active dispersal events and revert to a free-swimming, planktonic state to complete the biofilm life cycle. The signaling molecule nitric oxide (NO) was previously found to trigger biofilm dispersal in the opportunistic pathogen Pseudomonas aeruginosa at low, nontoxic concentrations (N. Barraud, D. J. Hassett, S. H. Hwang, S. A. Rice, S. Kjelleberg, and J. S. Webb, J. Bacteriol. 188:7344-7353, 2006).

NO was further shown to increase cell motility and susceptibility to antimicrobials. Recently, numerous studies revealed that increased degradation of the secondary messenger cyclic di-GMP (c-di-GMP) by specific phosphodiesterases (PDEs) triggers a planktonic mode of growth in eubacteria. In this study, the potential link between NO and c-di-GMP signaling was investigated by performing (i) PDE inhibitor studies, (ii) enzymatic assays to measure PDE activity, and (iii) direct quantification of intracellular c-di-GMP levels.

The results suggest a role for c-di-GMP signaling in triggering the biofilm dispersal event induced by NO, as dispersal requires PDE activity and addition of NO stimulates PDE and induces the concomitant decrease in intracellular c-di-GMP levels in P. aeruginosa. Furthermore, gene expression studies indicated global responses to low, nontoxic levels of NO in P. aeruginosa biofilms, including upregulation of genes involved in motility and energy metabolism and downregulation of adhesins and virulence factors.

Finally, site-directed mutagenesis of candidate genes and physiological characterization of the corresponding mutant strains uncovered that the chemotaxis transducer BdlA is involved in the biofilm dispersal response induced by NO.

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Published date: December 2009
Organisations: Biological Sciences

Identifiers

Local EPrints ID: 146303
URI: https://eprints.soton.ac.uk/id/eprint/146303
ISSN: 0021-9193
PURE UUID: 0639e933-0dbf-4da9-bb4e-42967811aef1
ORCID for Jeremy S. Webb: ORCID iD orcid.org/0000-0003-2068-8589

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Date deposited: 21 Apr 2010 09:42
Last modified: 12 Nov 2019 01:45

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