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.

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Main Authors: Rahimpour, Mehdi, Montero, Manuel, Almagro, Goizeder, Viale, Alejandro M., Muñoz Pérez, Francisco José, Baroja-Fernández, Edurne, Bahaji, Abdellatif, Eydallin, Gustavo, Pozueta Romero, Javier
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
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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
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