Specific Control of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface-Associated Behaviors by Two c-di-GMP Diguanylate Cyclases

ABSTRACT The signaling nucleotide cyclic diguanylate (c-di-GMP) regulates the transition between motile and sessile growth in a wide range of bacteria. Understanding how microbes control c-di-GMP metabolism to activate specific pathways is complicated by the apparent multifold redundancy of enzymes...

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Autores principales: Judith H. Merritt, Dae-Gon Ha, Kimberly N. Cowles, Wenyun Lu, Diana K. Morales, Joshua Rabinowitz, Zemer Gitai, George A. O’Toole
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Publicado: American Society for Microbiology 2010
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spelling oai:doaj.org-article:7e449232620047f1af042590d7ee8a032021-11-15T15:38:15ZSpecific Control of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface-Associated Behaviors by Two c-di-GMP Diguanylate Cyclases10.1128/mBio.00183-102150-7511https://doaj.org/article/7e449232620047f1af042590d7ee8a032010-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00183-10https://doaj.org/toc/2150-7511ABSTRACT The signaling nucleotide cyclic diguanylate (c-di-GMP) regulates the transition between motile and sessile growth in a wide range of bacteria. Understanding how microbes control c-di-GMP metabolism to activate specific pathways is complicated by the apparent multifold redundancy of enzymes that synthesize and degrade this dinucleotide, and several models have been proposed to explain how bacteria coordinate the actions of these many enzymes. Here we report the identification of a diguanylate cyclase (DGC), RoeA, of Pseudomonas aeruginosa that promotes the production of extracellular polysaccharide (EPS) and contributes to biofilm formation, that is, the transition from planktonic to surface-dwelling cells. Our studies reveal that RoeA and the previously described DGC SadC make distinct contributions to biofilm formation, controlling polysaccharide production and flagellar motility, respectively. Measurement of total cellular levels of c-di-GMP in ∆roeA and ∆sadC mutants in two different genetic backgrounds revealed no correlation between levels of c-di-GMP and the observed phenotypic output with regard to swarming motility and EPS production. Our data strongly argue against a model wherein changes in total levels of c-di-GMP can account for the specific surface-related phenotypes of P. aeruginosa. IMPORTANCE A critical question in the study of cyclic diguanylate (c-di-GMP) signaling is how the bacterial cell integrates contributions of multiple c-di-GMP-metabolizing enzymes to mediate its cognate functional outputs. One leading model suggests that the effects of c-di-GMP must, in part, be localized subcellularly. The data presented here show that the phenotypes controlled by two different diguanylate cyclase (DGC) enzymes have discrete outputs despite the same total level of c-di-GMP. These data support and extend the model in which localized c-di-GMP signaling likely contributes to coordination of the action of the multiple proteins involved in the synthesis, degradation, and/or binding of this critical signal.Judith H. MerrittDae-Gon HaKimberly N. CowlesWenyun LuDiana K. MoralesJoshua RabinowitzZemer GitaiGeorge A. O’TooleAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 1, Iss 4 (2010)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Judith H. Merritt
Dae-Gon Ha
Kimberly N. Cowles
Wenyun Lu
Diana K. Morales
Joshua Rabinowitz
Zemer Gitai
George A. O’Toole
Specific Control of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface-Associated Behaviors by Two c-di-GMP Diguanylate Cyclases
description ABSTRACT The signaling nucleotide cyclic diguanylate (c-di-GMP) regulates the transition between motile and sessile growth in a wide range of bacteria. Understanding how microbes control c-di-GMP metabolism to activate specific pathways is complicated by the apparent multifold redundancy of enzymes that synthesize and degrade this dinucleotide, and several models have been proposed to explain how bacteria coordinate the actions of these many enzymes. Here we report the identification of a diguanylate cyclase (DGC), RoeA, of Pseudomonas aeruginosa that promotes the production of extracellular polysaccharide (EPS) and contributes to biofilm formation, that is, the transition from planktonic to surface-dwelling cells. Our studies reveal that RoeA and the previously described DGC SadC make distinct contributions to biofilm formation, controlling polysaccharide production and flagellar motility, respectively. Measurement of total cellular levels of c-di-GMP in ∆roeA and ∆sadC mutants in two different genetic backgrounds revealed no correlation between levels of c-di-GMP and the observed phenotypic output with regard to swarming motility and EPS production. Our data strongly argue against a model wherein changes in total levels of c-di-GMP can account for the specific surface-related phenotypes of P. aeruginosa. IMPORTANCE A critical question in the study of cyclic diguanylate (c-di-GMP) signaling is how the bacterial cell integrates contributions of multiple c-di-GMP-metabolizing enzymes to mediate its cognate functional outputs. One leading model suggests that the effects of c-di-GMP must, in part, be localized subcellularly. The data presented here show that the phenotypes controlled by two different diguanylate cyclase (DGC) enzymes have discrete outputs despite the same total level of c-di-GMP. These data support and extend the model in which localized c-di-GMP signaling likely contributes to coordination of the action of the multiple proteins involved in the synthesis, degradation, and/or binding of this critical signal.
format article
author Judith H. Merritt
Dae-Gon Ha
Kimberly N. Cowles
Wenyun Lu
Diana K. Morales
Joshua Rabinowitz
Zemer Gitai
George A. O’Toole
author_facet Judith H. Merritt
Dae-Gon Ha
Kimberly N. Cowles
Wenyun Lu
Diana K. Morales
Joshua Rabinowitz
Zemer Gitai
George A. O’Toole
author_sort Judith H. Merritt
title Specific Control of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface-Associated Behaviors by Two c-di-GMP Diguanylate Cyclases
title_short Specific Control of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface-Associated Behaviors by Two c-di-GMP Diguanylate Cyclases
title_full Specific Control of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface-Associated Behaviors by Two c-di-GMP Diguanylate Cyclases
title_fullStr Specific Control of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface-Associated Behaviors by Two c-di-GMP Diguanylate Cyclases
title_full_unstemmed Specific Control of <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Surface-Associated Behaviors by Two c-di-GMP Diguanylate Cyclases
title_sort specific control of <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> surface-associated behaviors by two c-di-gmp diguanylate cyclases
publisher American Society for Microbiology
publishDate 2010
url https://doaj.org/article/7e449232620047f1af042590d7ee8a03
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