GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli
Escherichia coli glycogen metabolism involves the regulation of glgBXCAP operon expression and allosteric control of the GlgC [ADPG (ADP-glucose) pyrophosphorylase]-mediated catalysis of ATP and G1P (glucose-1-phosphate) to ADPG linked to glycogen biosynthesis. E. coli glycogen metabolism is also affected by glgS . Though the precise function of the protein it encodes is unknown, its deficiency causes both reduced glycogen content and enhanced levels of the GlgC-negative allosteric regulator AMP. The transcriptomic analyses carried out in the present study revealed that, compared with their isogenic BW25113 wild-type strain, glgS-null (ΔglgS) mutants have increased expression of the operons involved in the synthesis of type 1 fimbriae adhesins, flagella and nucleotides. In agreement, ΔglgS cells were hyperflagellated and hyperfimbriated, and displayed elevated swarming motility; these phenotypes all reverted to the wild-type by ectopic glgS expression. Also, ΔglgS cells accumulated high colanic acid content and displayed increased ability to form biofilms on polystyrene surfaces. F-driven conjugation based on large-scale interaction studies of glgS with all the non-essential genes of E. coli showed that deletion of purine biosynthesis genes complement the glycogen-deficient, high motility and high biofilm content phenotypes of ΔglgS cells. Overall the results of the present study indicate that glycogen deficiency in ΔglgS cells can be ascribed to high flagellar propulsion and high exopolysaccharide and purine nucleotides biosynthetic activities competing with GlgC for the same ATP and G1P pools. Supporting this proposal, glycogen-less ΔglgC cells displayed an elevated swarming motility, and accumulated high levels of colanic acid and biofilm. Furthermore, glgC overexpression reverted the glycogen-deficient, high swarming motility, high colanic acid and high biofilm content phenotypes of ΔglgS cells to the wild-type. As on the basis of the present study GlgS has emerged as a major determinant of E. coli surface composition and because its effect on glycogen metabolism appears to be only indirect, we propose to rename it as ScoR (surface composition regulator). © The Authors Journal compilation © 2013 Biochemical Society.
Main Authors: | , , , , , , , , |
---|---|
Format: | artículo biblioteca |
Published: |
Portland Press
2013-03-28
|
Subjects: | Biofilms, Exopolysaccharide, Flagellar motility, GlgS, Glycogen, Large-scale genetic interaction, Growth regulation, |
Online Access: | http://hdl.handle.net/10261/97518 |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
id |
dig-idab-es-10261-97518 |
---|---|
record_format |
koha |
spelling |
dig-idab-es-10261-975182016-09-08T09:55:40Z GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli Rahimpour, Mehdi Montero, Manuel Almagro, Goizeder Viale, Alejandro M. Muñoz Pérez, Francisco José Baroja-Fernández, Edurne Bahaji, Abdellatif Eydallin, Gustavo Pozueta Romero, Javier Biofilms Exopolysaccharide Flagellar motility GlgS Glycogen Large-scale genetic interaction Growth regulation Escherichia coli glycogen metabolism involves the regulation of glgBXCAP operon expression and allosteric control of the GlgC [ADPG (ADP-glucose) pyrophosphorylase]-mediated catalysis of ATP and G1P (glucose-1-phosphate) to ADPG linked to glycogen biosynthesis. E. coli glycogen metabolism is also affected by glgS . Though the precise function of the protein it encodes is unknown, its deficiency causes both reduced glycogen content and enhanced levels of the GlgC-negative allosteric regulator AMP. The transcriptomic analyses carried out in the present study revealed that, compared with their isogenic BW25113 wild-type strain, glgS-null (ΔglgS) mutants have increased expression of the operons involved in the synthesis of type 1 fimbriae adhesins, flagella and nucleotides. In agreement, ΔglgS cells were hyperflagellated and hyperfimbriated, and displayed elevated swarming motility; these phenotypes all reverted to the wild-type by ectopic glgS expression. Also, ΔglgS cells accumulated high colanic acid content and displayed increased ability to form biofilms on polystyrene surfaces. F-driven conjugation based on large-scale interaction studies of glgS with all the non-essential genes of E. coli showed that deletion of purine biosynthesis genes complement the glycogen-deficient, high motility and high biofilm content phenotypes of ΔglgS cells. Overall the results of the present study indicate that glycogen deficiency in ΔglgS cells can be ascribed to high flagellar propulsion and high exopolysaccharide and purine nucleotides biosynthetic activities competing with GlgC for the same ATP and G1P pools. Supporting this proposal, glycogen-less ΔglgC cells displayed an elevated swarming motility, and accumulated high levels of colanic acid and biofilm. Furthermore, glgC overexpression reverted the glycogen-deficient, high swarming motility, high colanic acid and high biofilm content phenotypes of ΔglgS cells to the wild-type. As on the basis of the present study GlgS has emerged as a major determinant of E. coli surface composition and because its effect on glycogen metabolism appears to be only indirect, we propose to rename it as ScoR (surface composition regulator). © The Authors Journal compilation © 2013 Biochemical Society. We thank Inigo Lasa and Cristina Solano for discussions and careful analysis of the paper and María Teresa Sesma and Maite Hidalgo (Institute of Agrobiotechnology, Navarra, Spain) for technical support. Peer Reviewed 2014-06-02T08:57:06Z 2014-06-02T08:57:06Z 2013-03-28 2014-06-02T08:57:06Z artículo http://purl.org/coar/resource_type/c_6501 doi: 10.1042/BJ20130154 issn: 0264-6021 Biochemical Journal 452: 559-573 (2013) http://hdl.handle.net/10261/97518 10.1042/BJ20130154 none Portland Press |
institution |
IDAB ES |
collection |
DSpace |
country |
España |
countrycode |
ES |
component |
Bibliográfico |
access |
En linea |
databasecode |
dig-idab-es |
tag |
biblioteca |
region |
Europa del Sur |
libraryname |
Biblioteca del IDAB España |
topic |
Biofilms Exopolysaccharide Flagellar motility GlgS Glycogen Large-scale genetic interaction Growth regulation Biofilms Exopolysaccharide Flagellar motility GlgS Glycogen Large-scale genetic interaction Growth regulation |
spellingShingle |
Biofilms Exopolysaccharide Flagellar motility GlgS Glycogen Large-scale genetic interaction Growth regulation Biofilms Exopolysaccharide Flagellar motility GlgS Glycogen Large-scale genetic interaction Growth regulation Rahimpour, Mehdi Montero, Manuel Almagro, Goizeder Viale, Alejandro M. Muñoz Pérez, Francisco José Baroja-Fernández, Edurne Bahaji, Abdellatif Eydallin, Gustavo Pozueta Romero, Javier GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli |
description |
Escherichia coli glycogen metabolism involves the regulation of glgBXCAP operon expression and allosteric control of the GlgC [ADPG (ADP-glucose) pyrophosphorylase]-mediated catalysis of ATP and G1P (glucose-1-phosphate) to ADPG linked to glycogen biosynthesis. E. coli glycogen metabolism is also affected by glgS . Though the precise function of the protein it encodes is unknown, its deficiency causes both reduced glycogen content and enhanced levels of the GlgC-negative allosteric regulator AMP. The transcriptomic analyses carried out in the present study revealed that, compared with their isogenic BW25113 wild-type strain, glgS-null (ΔglgS) mutants have increased expression of the operons involved in the synthesis of type 1 fimbriae adhesins, flagella and nucleotides. In agreement, ΔglgS cells were hyperflagellated and hyperfimbriated, and displayed elevated swarming motility; these phenotypes all reverted to the wild-type by ectopic glgS expression. Also, ΔglgS cells accumulated high colanic acid content and displayed increased ability to form biofilms on polystyrene surfaces. F-driven conjugation based on large-scale interaction studies of glgS with all the non-essential genes of E. coli showed that deletion of purine biosynthesis genes complement the glycogen-deficient, high motility and high biofilm content phenotypes of ΔglgS cells. Overall the results of the present study indicate that glycogen deficiency in ΔglgS cells can be ascribed to high flagellar propulsion and high exopolysaccharide and purine nucleotides biosynthetic activities competing with GlgC for the same ATP and G1P pools. Supporting this proposal, glycogen-less ΔglgC cells displayed an elevated swarming motility, and accumulated high levels of colanic acid and biofilm. Furthermore, glgC overexpression reverted the glycogen-deficient, high swarming motility, high colanic acid and high biofilm content phenotypes of ΔglgS cells to the wild-type. As on the basis of the present study GlgS has emerged as a major determinant of E. coli surface composition and because its effect on glycogen metabolism appears to be only indirect, we propose to rename it as ScoR (surface composition regulator). © The Authors Journal compilation © 2013 Biochemical Society. |
format |
artículo |
topic_facet |
Biofilms Exopolysaccharide Flagellar motility GlgS Glycogen Large-scale genetic interaction Growth regulation |
author |
Rahimpour, Mehdi Montero, Manuel Almagro, Goizeder Viale, Alejandro M. Muñoz Pérez, Francisco José Baroja-Fernández, Edurne Bahaji, Abdellatif Eydallin, Gustavo Pozueta Romero, Javier |
author_facet |
Rahimpour, Mehdi Montero, Manuel Almagro, Goizeder Viale, Alejandro M. Muñoz Pérez, Francisco José Baroja-Fernández, Edurne Bahaji, Abdellatif Eydallin, Gustavo Pozueta Romero, Javier |
author_sort |
Rahimpour, Mehdi |
title |
GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli |
title_short |
GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli |
title_full |
GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli |
title_fullStr |
GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli |
title_full_unstemmed |
GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli |
title_sort |
glgs, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in escherichia coli |
publisher |
Portland Press |
publishDate |
2013-03-28 |
url |
http://hdl.handle.net/10261/97518 |
work_keys_str_mv |
AT rahimpourmehdi glgsdescribedpreviouslyasaglycogensynthesiscontrolproteinnegativelyregulatesmotilityandbiofilmformationinescherichiacoli AT monteromanuel glgsdescribedpreviouslyasaglycogensynthesiscontrolproteinnegativelyregulatesmotilityandbiofilmformationinescherichiacoli AT almagrogoizeder glgsdescribedpreviouslyasaglycogensynthesiscontrolproteinnegativelyregulatesmotilityandbiofilmformationinescherichiacoli AT vialealejandrom glgsdescribedpreviouslyasaglycogensynthesiscontrolproteinnegativelyregulatesmotilityandbiofilmformationinescherichiacoli AT munozperezfranciscojose glgsdescribedpreviouslyasaglycogensynthesiscontrolproteinnegativelyregulatesmotilityandbiofilmformationinescherichiacoli AT barojafernandezedurne glgsdescribedpreviouslyasaglycogensynthesiscontrolproteinnegativelyregulatesmotilityandbiofilmformationinescherichiacoli AT bahajiabdellatif glgsdescribedpreviouslyasaglycogensynthesiscontrolproteinnegativelyregulatesmotilityandbiofilmformationinescherichiacoli AT eydallingustavo glgsdescribedpreviouslyasaglycogensynthesiscontrolproteinnegativelyregulatesmotilityandbiofilmformationinescherichiacoli AT pozuetaromerojavier glgsdescribedpreviouslyasaglycogensynthesiscontrolproteinnegativelyregulatesmotilityandbiofilmformationinescherichiacoli |
_version_ |
1777663440426369024 |