BolA Is Required for the Accurate Regulation of c-di-GMP, a Central Player in Biofilm Formation

ABSTRACT The bacterial second messenger cyclic dimeric GMP (c-di-GMP) is a nearly ubiquitous intracellular signaling molecule involved in the transition from the motile to the sessile/biofilm state in bacteria. C-di-GMP regulates various cellular processes, including biofilm formation, motility, and...

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Autores principales:	Ricardo N. Moreira, Clémentine Dressaire, Susana Barahona, Lisete Galego, Volkhard Kaever, Urs Jenal, Cecília M. Arraiano
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	biofilm BolA diguanylate cyclase motility phosphodiesterase c-di-GMP Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5175c879c1c9439ea3215bd0846103e5
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spelling	oai:doaj.org-article:5175c879c1c9439ea3215bd0846103e52021-11-15T15:51:51ZBolA Is Required for the Accurate Regulation of c-di-GMP, a Central Player in Biofilm Formation10.1128/mBio.00443-172150-7511https://doaj.org/article/5175c879c1c9439ea3215bd0846103e52017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00443-17https://doaj.org/toc/2150-7511ABSTRACT The bacterial second messenger cyclic dimeric GMP (c-di-GMP) is a nearly ubiquitous intracellular signaling molecule involved in the transition from the motile to the sessile/biofilm state in bacteria. C-di-GMP regulates various cellular processes, including biofilm formation, motility, and virulence. BolA is a transcription factor that promotes survival in different stresses and is also involved in biofilm formation. Both BolA and c-di-GMP participate in the regulation of motility mechanisms leading to similar phenotypes. Here, we establish the importance of the balance between these two factors for accurate regulation of the transition between the planktonic and sessile lifestyles. This balance is achieved by negative-feedback regulation of BolA and c-di-GMP. BolA not only contributes directly to the motility of bacteria but also regulates the expression of diguanylate cyclases and phosphodiesterases. This expression modulation influences the synthesis and degradation of c-di-GMP, while this signaling metabolite has a negative influence in bolA mRNA transcription. Finally, we present evidence of the dominant role of BolA in biofilm, showing that, even in the presence of elevated c-di-GMP levels, biofilm formation is reduced in the absence of BolA. C-di-GMP is one of the most important bacterial second messengers involved in several cellular processes, including virulence, cell cycle regulation, biofilm formation, and flagellar synthesis. In this study, we unravelled a direct connection between the bolA morphogene and the c-di-GMP signaling molecule. We show the important cross-talk that occurs between these two molecular regulators during the transition between the motile/planktonic and adhesive/sessile lifestyles in Escherichia coli. This work provides important clues that can be helpful in the development of new strategies, and the results can be applied to other organisms with relevance for human health. IMPORTANCE Bacterial cells have evolved several mechanisms to cope with environmental stresses. BolA-like proteins are widely conserved from prokaryotes to eukaryotes, and in Escherichia coli, in addition to its pleiotropic effects, this protein plays a determinant role in bacterial motility and biofilm formation regulation. Similarly, the bacterial second messenger c-di-GMP is a molecule with high importance in coordinating the switch between planktonic and sessile life in bacteria. Here we have unravelled the importance of accurate regulation of cross-talk between BolA and c-di-GMP for a proper response in the regulation of these bacterial lifestyles. This finding underlines the complexity of bacterial cell regulation, revealing the existence of one additional tool for fine-tuning such important cellular molecular mechanisms. The relationship between BolA and c-di-GMP gives new perspectives regarding biofilm formation and opens the possibility to extend our studies to other organisms with relevance for human health.Ricardo N. MoreiraClémentine DressaireSusana BarahonaLisete GalegoVolkhard KaeverUrs JenalCecília M. ArraianoAmerican Society for MicrobiologyarticlebiofilmBolAdiguanylate cyclasemotilityphosphodiesterasec-di-GMPMicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	biofilm BolA diguanylate cyclase motility phosphodiesterase c-di-GMP Microbiology QR1-502
spellingShingle	biofilm BolA diguanylate cyclase motility phosphodiesterase c-di-GMP Microbiology QR1-502 Ricardo N. Moreira Clémentine Dressaire Susana Barahona Lisete Galego Volkhard Kaever Urs Jenal Cecília M. Arraiano BolA Is Required for the Accurate Regulation of c-di-GMP, a Central Player in Biofilm Formation
description	ABSTRACT The bacterial second messenger cyclic dimeric GMP (c-di-GMP) is a nearly ubiquitous intracellular signaling molecule involved in the transition from the motile to the sessile/biofilm state in bacteria. C-di-GMP regulates various cellular processes, including biofilm formation, motility, and virulence. BolA is a transcription factor that promotes survival in different stresses and is also involved in biofilm formation. Both BolA and c-di-GMP participate in the regulation of motility mechanisms leading to similar phenotypes. Here, we establish the importance of the balance between these two factors for accurate regulation of the transition between the planktonic and sessile lifestyles. This balance is achieved by negative-feedback regulation of BolA and c-di-GMP. BolA not only contributes directly to the motility of bacteria but also regulates the expression of diguanylate cyclases and phosphodiesterases. This expression modulation influences the synthesis and degradation of c-di-GMP, while this signaling metabolite has a negative influence in bolA mRNA transcription. Finally, we present evidence of the dominant role of BolA in biofilm, showing that, even in the presence of elevated c-di-GMP levels, biofilm formation is reduced in the absence of BolA. C-di-GMP is one of the most important bacterial second messengers involved in several cellular processes, including virulence, cell cycle regulation, biofilm formation, and flagellar synthesis. In this study, we unravelled a direct connection between the bolA morphogene and the c-di-GMP signaling molecule. We show the important cross-talk that occurs between these two molecular regulators during the transition between the motile/planktonic and adhesive/sessile lifestyles in Escherichia coli. This work provides important clues that can be helpful in the development of new strategies, and the results can be applied to other organisms with relevance for human health. IMPORTANCE Bacterial cells have evolved several mechanisms to cope with environmental stresses. BolA-like proteins are widely conserved from prokaryotes to eukaryotes, and in Escherichia coli, in addition to its pleiotropic effects, this protein plays a determinant role in bacterial motility and biofilm formation regulation. Similarly, the bacterial second messenger c-di-GMP is a molecule with high importance in coordinating the switch between planktonic and sessile life in bacteria. Here we have unravelled the importance of accurate regulation of cross-talk between BolA and c-di-GMP for a proper response in the regulation of these bacterial lifestyles. This finding underlines the complexity of bacterial cell regulation, revealing the existence of one additional tool for fine-tuning such important cellular molecular mechanisms. The relationship between BolA and c-di-GMP gives new perspectives regarding biofilm formation and opens the possibility to extend our studies to other organisms with relevance for human health.
format	article
author	Ricardo N. Moreira Clémentine Dressaire Susana Barahona Lisete Galego Volkhard Kaever Urs Jenal Cecília M. Arraiano
author_facet	Ricardo N. Moreira Clémentine Dressaire Susana Barahona Lisete Galego Volkhard Kaever Urs Jenal Cecília M. Arraiano
author_sort	Ricardo N. Moreira
title	BolA Is Required for the Accurate Regulation of c-di-GMP, a Central Player in Biofilm Formation
title_short	BolA Is Required for the Accurate Regulation of c-di-GMP, a Central Player in Biofilm Formation
title_full	BolA Is Required for the Accurate Regulation of c-di-GMP, a Central Player in Biofilm Formation
title_fullStr	BolA Is Required for the Accurate Regulation of c-di-GMP, a Central Player in Biofilm Formation
title_full_unstemmed	BolA Is Required for the Accurate Regulation of c-di-GMP, a Central Player in Biofilm Formation
title_sort	bola is required for the accurate regulation of c-di-gmp, a central player in biofilm formation
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/5175c879c1c9439ea3215bd0846103e5
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BolA Is Required for the Accurate Regulation of c-di-GMP, a Central Player in Biofilm Formation

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