Cohesive Properties of the <italic toggle="yes">Caulobacter crescentus</italic> Holdfast Adhesin Are Regulated by a Novel c-di-GMP Effector Protein
ABSTRACT When encountering surfaces, many bacteria produce adhesins to facilitate their initial attachment and to irreversibly glue themselves to the solid substrate. A central molecule regulating the processes of this motile-sessile transition is the second messenger c-di-GMP, which stimulates the...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2017-05-01
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| Series: | mBio |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.00294-17 |
| _version_ | 1818739470453702656 |
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| author | Kathrin S. Sprecher Isabelle Hug Jutta Nesper Eva Potthoff Mohamed-Ali Mahi Matteo Sangermani Volkhard Kaever Torsten Schwede Julia Vorholt Urs Jenal |
| author_facet | Kathrin S. Sprecher Isabelle Hug Jutta Nesper Eva Potthoff Mohamed-Ali Mahi Matteo Sangermani Volkhard Kaever Torsten Schwede Julia Vorholt Urs Jenal |
| author_sort | Kathrin S. Sprecher |
| collection | DOAJ |
| description | ABSTRACT When encountering surfaces, many bacteria produce adhesins to facilitate their initial attachment and to irreversibly glue themselves to the solid substrate. A central molecule regulating the processes of this motile-sessile transition is the second messenger c-di-GMP, which stimulates the production of a variety of exopolysaccharide adhesins in different bacterial model organisms. In Caulobacter crescentus, c-di-GMP regulates the synthesis of the polar holdfast adhesin during the cell cycle, yet the molecular and cellular details of this control are currently unknown. Here we identify HfsK, a member of a versatile N-acetyltransferase family, as a novel c-di-GMP effector involved in holdfast biogenesis. Cells lacking HfsK form highly malleable holdfast structures with reduced adhesive strength that cannot support surface colonization. We present indirect evidence that HfsK modifies the polysaccharide component of holdfast to buttress its cohesive properties. HfsK is a soluble protein but associates with the cell membrane during most of the cell cycle. Coincident with peak c-di-GMP levels during the C. crescentus cell cycle, HfsK relocalizes to the cytosol in a c-di-GMP-dependent manner. Our results indicate that this c-di-GMP-mediated dynamic positioning controls HfsK activity, leading to its inactivation at high c-di-GMP levels. A short C-terminal extension is essential for the membrane association, c-di-GMP binding, and activity of HfsK. We propose a model in which c-di-GMP binding leads to the dispersal and inactivation of HfsK as part of holdfast biogenesis progression. IMPORTANCE Exopolysaccharide (EPS) adhesins are important determinants of bacterial surface colonization and biofilm formation. Biofilms are a major cause of chronic infections and are responsible for biofouling on water-exposed surfaces. To tackle these problems, it is essential to dissect the processes leading to surface colonization at the molecular and cellular levels. Here we describe a novel c-di-GMP effector, HfsK, that contributes to the cohesive properties and stability of the holdfast adhesin in C. crescentus. We demonstrate for the first time that c-di-GMP, in addition to its role in the regulation of the rate of EPS production, also modulates the physicochemical properties of bacterial adhesins. By demonstrating how c-di-GMP coordinates the activity and subcellular localization of HfsK, we provide a novel understanding of the cellular processes involved in adhesin biogenesis control. Homologs of HfsK are found in representatives of different bacterial phyla, suggesting that they play important roles in various EPS synthesis systems. |
| first_indexed | 2024-12-18T01:25:21Z |
| format | Article |
| id | doaj.art-6885bc0814574df99650f49ba6e8fef8 |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T01:25:21Z |
| publishDate | 2017-05-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-6885bc0814574df99650f49ba6e8fef82022-12-21T21:25:44ZengAmerican Society for MicrobiologymBio2150-75112017-05-018210.1128/mBio.00294-17Cohesive Properties of the <italic toggle="yes">Caulobacter crescentus</italic> Holdfast Adhesin Are Regulated by a Novel c-di-GMP Effector ProteinKathrin S. Sprecher0Isabelle Hug1Jutta Nesper2Eva Potthoff3Mohamed-Ali Mahi4Matteo Sangermani5Volkhard Kaever6Torsten Schwede7Julia Vorholt8Urs Jenal9Focal Area of Infection Biology, Biozentrum, University of Basel, Basel, SwitzerlandFocal Area of Infection Biology, Biozentrum, University of Basel, Basel, SwitzerlandFocal Area of Infection Biology, Biozentrum, University of Basel, Basel, SwitzerlandInstitute of Microbiology, ETH Zurich, Zurich, SwitzerlandFocal Area of Computational & Systems Biology, Biozentrum, University of Basel, Basel, SwitzerlandFocal Area of Infection Biology, Biozentrum, University of Basel, Basel, SwitzerlandResearch Core Unit Metabolomics and Institute of Pharmacology, Hannover Medical School, Hannover, GermanyFocal Area of Computational & Systems Biology, Biozentrum, University of Basel, Basel, SwitzerlandInstitute of Microbiology, ETH Zurich, Zurich, SwitzerlandFocal Area of Infection Biology, Biozentrum, University of Basel, Basel, SwitzerlandABSTRACT When encountering surfaces, many bacteria produce adhesins to facilitate their initial attachment and to irreversibly glue themselves to the solid substrate. A central molecule regulating the processes of this motile-sessile transition is the second messenger c-di-GMP, which stimulates the production of a variety of exopolysaccharide adhesins in different bacterial model organisms. In Caulobacter crescentus, c-di-GMP regulates the synthesis of the polar holdfast adhesin during the cell cycle, yet the molecular and cellular details of this control are currently unknown. Here we identify HfsK, a member of a versatile N-acetyltransferase family, as a novel c-di-GMP effector involved in holdfast biogenesis. Cells lacking HfsK form highly malleable holdfast structures with reduced adhesive strength that cannot support surface colonization. We present indirect evidence that HfsK modifies the polysaccharide component of holdfast to buttress its cohesive properties. HfsK is a soluble protein but associates with the cell membrane during most of the cell cycle. Coincident with peak c-di-GMP levels during the C. crescentus cell cycle, HfsK relocalizes to the cytosol in a c-di-GMP-dependent manner. Our results indicate that this c-di-GMP-mediated dynamic positioning controls HfsK activity, leading to its inactivation at high c-di-GMP levels. A short C-terminal extension is essential for the membrane association, c-di-GMP binding, and activity of HfsK. We propose a model in which c-di-GMP binding leads to the dispersal and inactivation of HfsK as part of holdfast biogenesis progression. IMPORTANCE Exopolysaccharide (EPS) adhesins are important determinants of bacterial surface colonization and biofilm formation. Biofilms are a major cause of chronic infections and are responsible for biofouling on water-exposed surfaces. To tackle these problems, it is essential to dissect the processes leading to surface colonization at the molecular and cellular levels. Here we describe a novel c-di-GMP effector, HfsK, that contributes to the cohesive properties and stability of the holdfast adhesin in C. crescentus. We demonstrate for the first time that c-di-GMP, in addition to its role in the regulation of the rate of EPS production, also modulates the physicochemical properties of bacterial adhesins. By demonstrating how c-di-GMP coordinates the activity and subcellular localization of HfsK, we provide a novel understanding of the cellular processes involved in adhesin biogenesis control. Homologs of HfsK are found in representatives of different bacterial phyla, suggesting that they play important roles in various EPS synthesis systems.https://journals.asm.org/doi/10.1128/mBio.00294-17 |
| spellingShingle | Kathrin S. Sprecher Isabelle Hug Jutta Nesper Eva Potthoff Mohamed-Ali Mahi Matteo Sangermani Volkhard Kaever Torsten Schwede Julia Vorholt Urs Jenal Cohesive Properties of the <italic toggle="yes">Caulobacter crescentus</italic> Holdfast Adhesin Are Regulated by a Novel c-di-GMP Effector Protein mBio |
| title | Cohesive Properties of the <italic toggle="yes">Caulobacter crescentus</italic> Holdfast Adhesin Are Regulated by a Novel c-di-GMP Effector Protein |
| title_full | Cohesive Properties of the <italic toggle="yes">Caulobacter crescentus</italic> Holdfast Adhesin Are Regulated by a Novel c-di-GMP Effector Protein |
| title_fullStr | Cohesive Properties of the <italic toggle="yes">Caulobacter crescentus</italic> Holdfast Adhesin Are Regulated by a Novel c-di-GMP Effector Protein |
| title_full_unstemmed | Cohesive Properties of the <italic toggle="yes">Caulobacter crescentus</italic> Holdfast Adhesin Are Regulated by a Novel c-di-GMP Effector Protein |
| title_short | Cohesive Properties of the <italic toggle="yes">Caulobacter crescentus</italic> Holdfast Adhesin Are Regulated by a Novel c-di-GMP Effector Protein |
| title_sort | cohesive properties of the italic toggle yes caulobacter crescentus italic holdfast adhesin are regulated by a novel c di gmp effector protein |
| url | https://journals.asm.org/doi/10.1128/mBio.00294-17 |
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