Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Christina Pesavento
  • Gisela Becker
  • Nicole Sommerfeldt
  • Alexandra Possling
  • Natalia Tschowri
  • Anika Mehlis
  • Regine Hengge

External Research Organisations

  • Freie Universität Berlin (FU Berlin)
View graph of relations

Details

Original languageEnglish
Pages (from-to)2434-46
Number of pages13
JournalGenes & development
Volume22
Issue number17
Publication statusPublished - 1 Sept 2008
Externally publishedYes

Abstract

During the transition from post-exponential to stationary phase, Escherichia coli changes from the motile-planktonic to the adhesive-sedentary "lifestyle." We demonstrate this transition to be controlled by mutual inhibition of the FlhDC/motility and sigma(S)/adhesion control cascades at two distinct hierarchical levels. At the top level, motility gene expression and the general stress response are inversely coordinated by sigma(70)/sigma(FliA)/sigma(S) competition for core RNA polymerase and the FlhDC-controlled FliZ protein acting as a sigma(S) inhibitor. At a lower level, the signaling molecule bis-(3'-5')-cyclic-diguanosine monophosphate (c-di-GMP) reduces flagellar activity and stimulates transcription of csgD, which encodes an essential activator of adhesive curli fimbriae expression. This c-di-GMP is antagonistically controlled by sigma(S)-regulated GGDEF proteins (mainly YegE) and YhjH, an EAL protein and c-di-GMP phosphodiesterase under FlhDC/FliA control. The switch from motility-based foraging to the general stress response and curli expression requires sigma(S)-modulated down-regulation of expression of the flagellar regulatory cascade as well as proteolysis of the flagellar master regulator FlhDC. Control of YhjH by FlhDC and of YegE by sigma(S) produces a fine-tuned checkpoint system that "unlocks" curli expression only after down-regulation of flagellar gene expression. In summary, these data reveal the logic and sequence of molecular events underlying the motile-to-adhesive "lifestyle" switch in E. coli.

Keywords

    Cyclic GMP/analogs & derivatives, Escherichia coli K12/physiology, Escherichia coli Proteins/metabolism, Fimbriae, Bacterial/physiology, Flagella/physiology, Gene Expression Regulation, Bacterial, Phosphoric Diester Hydrolases/metabolism, Trans-Activators/metabolism

Cite this

Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. / Pesavento, Christina; Becker, Gisela; Sommerfeldt, Nicole et al.
In: Genes & development, Vol. 22, No. 17, 01.09.2008, p. 2434-46.

Research output: Contribution to journalArticleResearchpeer review

Pesavento, C, Becker, G, Sommerfeldt, N, Possling, A, Tschowri, N, Mehlis, A & Hengge, R 2008, 'Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli', Genes & development, vol. 22, no. 17, pp. 2434-46. https://doi.org/10.1101/gad.475808
Pesavento, C., Becker, G., Sommerfeldt, N., Possling, A., Tschowri, N., Mehlis, A., & Hengge, R. (2008). Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes & development, 22(17), 2434-46. https://doi.org/10.1101/gad.475808
Pesavento C, Becker G, Sommerfeldt N, Possling A, Tschowri N, Mehlis A et al. Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes & development. 2008 Sept 1;22(17):2434-46. doi: 10.1101/gad.475808
Pesavento, Christina ; Becker, Gisela ; Sommerfeldt, Nicole et al. / Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. In: Genes & development. 2008 ; Vol. 22, No. 17. pp. 2434-46.
Download
@article{7b32ffd913194fe78f56c91db6b9e0bd,
title = "Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli",
abstract = "During the transition from post-exponential to stationary phase, Escherichia coli changes from the motile-planktonic to the adhesive-sedentary {"}lifestyle.{"} We demonstrate this transition to be controlled by mutual inhibition of the FlhDC/motility and sigma(S)/adhesion control cascades at two distinct hierarchical levels. At the top level, motility gene expression and the general stress response are inversely coordinated by sigma(70)/sigma(FliA)/sigma(S) competition for core RNA polymerase and the FlhDC-controlled FliZ protein acting as a sigma(S) inhibitor. At a lower level, the signaling molecule bis-(3'-5')-cyclic-diguanosine monophosphate (c-di-GMP) reduces flagellar activity and stimulates transcription of csgD, which encodes an essential activator of adhesive curli fimbriae expression. This c-di-GMP is antagonistically controlled by sigma(S)-regulated GGDEF proteins (mainly YegE) and YhjH, an EAL protein and c-di-GMP phosphodiesterase under FlhDC/FliA control. The switch from motility-based foraging to the general stress response and curli expression requires sigma(S)-modulated down-regulation of expression of the flagellar regulatory cascade as well as proteolysis of the flagellar master regulator FlhDC. Control of YhjH by FlhDC and of YegE by sigma(S) produces a fine-tuned checkpoint system that {"}unlocks{"} curli expression only after down-regulation of flagellar gene expression. In summary, these data reveal the logic and sequence of molecular events underlying the motile-to-adhesive {"}lifestyle{"} switch in E. coli.",
keywords = "Cyclic GMP/analogs & derivatives, Escherichia coli K12/physiology, Escherichia coli Proteins/metabolism, Fimbriae, Bacterial/physiology, Flagella/physiology, Gene Expression Regulation, Bacterial, Phosphoric Diester Hydrolases/metabolism, Trans-Activators/metabolism",
author = "Christina Pesavento and Gisela Becker and Nicole Sommerfeldt and Alexandra Possling and Natalia Tschowri and Anika Mehlis and Regine Hengge",
year = "2008",
month = sep,
day = "1",
doi = "10.1101/gad.475808",
language = "English",
volume = "22",
pages = "2434--46",
journal = "Genes & development",
issn = "0890-9369",
publisher = "Cold Spring Harbor Laboratory Press",
number = "17",

}

Download

TY - JOUR

T1 - Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli

AU - Pesavento, Christina

AU - Becker, Gisela

AU - Sommerfeldt, Nicole

AU - Possling, Alexandra

AU - Tschowri, Natalia

AU - Mehlis, Anika

AU - Hengge, Regine

PY - 2008/9/1

Y1 - 2008/9/1

N2 - During the transition from post-exponential to stationary phase, Escherichia coli changes from the motile-planktonic to the adhesive-sedentary "lifestyle." We demonstrate this transition to be controlled by mutual inhibition of the FlhDC/motility and sigma(S)/adhesion control cascades at two distinct hierarchical levels. At the top level, motility gene expression and the general stress response are inversely coordinated by sigma(70)/sigma(FliA)/sigma(S) competition for core RNA polymerase and the FlhDC-controlled FliZ protein acting as a sigma(S) inhibitor. At a lower level, the signaling molecule bis-(3'-5')-cyclic-diguanosine monophosphate (c-di-GMP) reduces flagellar activity and stimulates transcription of csgD, which encodes an essential activator of adhesive curli fimbriae expression. This c-di-GMP is antagonistically controlled by sigma(S)-regulated GGDEF proteins (mainly YegE) and YhjH, an EAL protein and c-di-GMP phosphodiesterase under FlhDC/FliA control. The switch from motility-based foraging to the general stress response and curli expression requires sigma(S)-modulated down-regulation of expression of the flagellar regulatory cascade as well as proteolysis of the flagellar master regulator FlhDC. Control of YhjH by FlhDC and of YegE by sigma(S) produces a fine-tuned checkpoint system that "unlocks" curli expression only after down-regulation of flagellar gene expression. In summary, these data reveal the logic and sequence of molecular events underlying the motile-to-adhesive "lifestyle" switch in E. coli.

AB - During the transition from post-exponential to stationary phase, Escherichia coli changes from the motile-planktonic to the adhesive-sedentary "lifestyle." We demonstrate this transition to be controlled by mutual inhibition of the FlhDC/motility and sigma(S)/adhesion control cascades at two distinct hierarchical levels. At the top level, motility gene expression and the general stress response are inversely coordinated by sigma(70)/sigma(FliA)/sigma(S) competition for core RNA polymerase and the FlhDC-controlled FliZ protein acting as a sigma(S) inhibitor. At a lower level, the signaling molecule bis-(3'-5')-cyclic-diguanosine monophosphate (c-di-GMP) reduces flagellar activity and stimulates transcription of csgD, which encodes an essential activator of adhesive curli fimbriae expression. This c-di-GMP is antagonistically controlled by sigma(S)-regulated GGDEF proteins (mainly YegE) and YhjH, an EAL protein and c-di-GMP phosphodiesterase under FlhDC/FliA control. The switch from motility-based foraging to the general stress response and curli expression requires sigma(S)-modulated down-regulation of expression of the flagellar regulatory cascade as well as proteolysis of the flagellar master regulator FlhDC. Control of YhjH by FlhDC and of YegE by sigma(S) produces a fine-tuned checkpoint system that "unlocks" curli expression only after down-regulation of flagellar gene expression. In summary, these data reveal the logic and sequence of molecular events underlying the motile-to-adhesive "lifestyle" switch in E. coli.

KW - Cyclic GMP/analogs & derivatives

KW - Escherichia coli K12/physiology

KW - Escherichia coli Proteins/metabolism

KW - Fimbriae, Bacterial/physiology

KW - Flagella/physiology

KW - Gene Expression Regulation, Bacterial

KW - Phosphoric Diester Hydrolases/metabolism

KW - Trans-Activators/metabolism

U2 - 10.1101/gad.475808

DO - 10.1101/gad.475808

M3 - Article

C2 - 18765794

VL - 22

SP - 2434

EP - 2446

JO - Genes & development

JF - Genes & development

SN - 0890-9369

IS - 17

ER -

By the same author(s)