Logical-continuous modelling of post-translationally regulated bistability of curli fiber expression in Escherichia coli

Yousef, Kaveh Pouran; Streck, Adam; Schütte, Christof; Siebert, Heike; Hengge, Regine; Kleist, Max von

doi:10.1186/s12918-015-0183-x

Cited by 13 publications

(14 citation statements)

References 52 publications

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“…Even more intriguingly, we also observed a minor subpopulation of cells with high curli expression but low σ S activity. These results suggest that bimodality in curli expression arises due to the regulation downstream from σ S , most probably at the level of CsgD ( Grantcharova et al, 2010 ; Yousef et al, 2015 ), and that the curli-ON switch can be achieved already prior to the full activation of σ S . Notably, csgD expression is either directly or indirectly regulated by a number of cellular factors, including different transcription factors, levels of second messenger cyclic diguanosine monophosphate (cyclic di-GMP) and small regulatory RNAs (sRNAs) that mediate cellular responses to diverse environmental changes ( Gerstel and Römling, 2003 ; Jubelin et al, 2005 ; Pesavento and Hengge, 2009 ; Ishihama, 2010 ; Ogasawara et al, 2010a ; Liu et al, 2014 ; Michaux et al, 2014 ; Mika and Hengge, 2014 ).…”

Section: Discussionmentioning

confidence: 88%

Diversification of Gene Expression during Formation of Static Submerged Biofilms by Escherichia coli

et al. 2016

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Many bacteria primarily exist in nature as structured multicellular communities, so called biofilms. Biofilm formation is a highly regulated process that includes the transition from the motile planktonic to sessile biofilm lifestyle. Cellular differentiation within a biofilm is a commonly accepted concept but it remains largely unclear when, where and how exactly such differentiation arises. Here we used fluorescent transcriptional reporters to quantitatively analyze spatio-temporal expression patterns of several groups of genes during the formation of submerged Escherichia coli biofilms in an open static system. We first confirm that formation of such submerged biofilms as well as pellicles at the liquid-air interface requires the major matrix component, curli, and flagella-mediated motility. We further demonstrate that in this system, diversification of gene expression leads to emergence of at least three distinct subpopulations of E. coli, which differ in their levels of curli and flagella expression, and in the activity of the stationary phase sigma factor σS. Our study reveals mutually exclusive expression of curli fibers and flagella at the single cell level, with high curli levels being confined to dense cell aggregates/microcolonies and flagella expression showing an opposite expression pattern. Interestingly, despite the known σS-dependence of curli induction, there was only a partial correlation between the σS activity and curli expression, with subpopulations of cells having high σS activity but low curli expression and vice versa. Finally, consistent with different physiology of the observed subpopulations, we show striking differences between the growth rates of cells within and outside of aggregates.

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Section: Discussionmentioning

confidence: 88%

Diversification of Gene Expression during Formation of Static Submerged Biofilms by Escherichia coli

et al. 2016

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“…Direct interactions between PdeR and DgcM and their key functions for the molecular switch that turns on CsgD expression ( Fig. 1E ) have been previously analyzed in great detail ( 13 , 14 , 39 ). While it was clear that DgcE acts directly upstream of PdeR and provides the major positive input into this switch ( 13 , 17 , 20 ), the multiple direct protein interactions of DgcE in the c-di-GMP signaling supermodule indicate that this c-di-GMP input is specific and local also.…”

Section: Discussionmentioning

confidence: 99%

“…It is also conceivable that PdeR and DgcE could directly inhibit each other, which would contribute to the positive-feedback loops ( Fig. 1E ) that confer bistable switch properties to this system ( 39 ). Notably, DgcE is one of four DGCs that can interact with PdeR ( Fig.…”

Section: Discussionmentioning

confidence: 99%

More than Enzymes That Make or Break Cyclic Di-GMP—Local Signaling in the Interactome of GGDEF/EAL Domain Proteins of Escherichia coli

Sarenko

Klauck

Wilke

et al. 2017

mBio

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128

197

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The bacterial second messenger bis-(3′-5′)-cyclic diguanosine monophosphate (c-di-GMP) ubiquitously promotes bacterial biofilm formation. Intracellular pools of c-di-GMP seem to be dynamically negotiated by diguanylate cyclases (DGCs, with GGDEF domains) and specific phosphodiesterases (PDEs, with EAL or HD-GYP domains). Most bacterial species possess multiple DGCs and PDEs, often with surprisingly distinct and specific output functions. One explanation for such specificity is “local” c-di-GMP signaling, which is believed to involve direct interactions between specific DGC/PDE pairs and c-di-GMP-binding effector/target systems. Here we present a systematic analysis of direct protein interactions among all 29 GGDEF/EAL domain proteins of Escherichia coli. Since the effects of interactions depend on coexpression and stoichiometries, cellular levels of all GGDEF/EAL domain proteins were also quantified and found to vary dynamically along the growth cycle. Instead of detecting specific pairs of interacting DGCs and PDEs, we discovered a tightly interconnected protein network of a specific subset or “supermodule” of DGCs and PDEs with a coregulated core of five hyperconnected hub proteins. These include the DGC/PDE proteins representing the c-di-GMP switch that turns on biofilm matrix production in E. coli. Mutants lacking these core hub proteins show drastic biofilm-related phenotypes but no changes in cellular c-di-GMP levels. Overall, our results provide the basis for a novel model of local c-di-GMP signaling in which a single strongly expressed master PDE, PdeH, dynamically eradicates global effects of several DGCs by strongly draining the global c-di-GMP pool and thereby restricting these DGCs to serving as local c-di-GMP sources that activate specific colocalized effector/target systems.

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“…Mathematical modelling indicated that the DgcE/PdeR/DgcM/MlrA-mediated c-di-GMP control module can operate as a bistable switch [ 72 ]. The major ingredients generating such behaviour are two feedback loops that stabilize the OFF and ON states, respectively, in csgD transcription ( figure 2 ): (i) PdeR degrades the inhibitor, i.e.…”

Section: Pder: a Trigger Pde Throws The Switch To Turn On Biofilm Matmentioning

confidence: 99%

Trigger phosphodiesterases as a novel class of c-di-GMP effector proteins

Hengge¹

2016

Phil. Trans. R. Soc. B

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The bacterial second messenger c-di-GMP controls bacterial biofilm formation, motility, cell cycle progression, development and virulence. It is synthesized by diguanylate cyclases (with GGDEF domains), degraded by specific phosphodiesterases (PDEs, with EAL of HD-GYP domains) and sensed by a wide variety of c-di-GMP-binding effectors that control diverse targets. c-di-GMP-binding effectors can be riboswitches as well as proteins with highly diverse structures and functions. The latter include ‘degenerate’ GGDEF/EAL domain proteins that are enzymatically inactive but still able to bind c-di-GMP. Surprisingly, two enzymatically active ‘trigger PDEs’, the Escherichia coli proteins PdeR and PdeL, have recently been added to this list of c-di-GMP-sensing effectors. Mechanistically, trigger PDEs are multifunctional. They directly and specifically interact with a macromolecular target (e.g. with a transcription factor or directly with a promoter region), whose activity they control by their binding and degradation of c-di-GMP—their PDE activity thus represents the c-di-GMP sensor or effector function. In this process, c-di-GMP serves as a regulatory ligand, but in contrast to classical allosteric control, this ligand is also degraded. The resulting kinetics and circuitry of control are ideally suited for trigger PDEs to serve as key components in regulatory switches.This article is part of the themed issue ‘The new bacteriology’.

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Logical-continuous modelling of post-translationally regulated bistability of curli fiber expression in Escherichia coli

Cited by 13 publications

References 52 publications

Diversification of Gene Expression during Formation of Static Submerged Biofilms by Escherichia coli

Diversification of Gene Expression during Formation of Static Submerged Biofilms by Escherichia coli

More than Enzymes That Make or Break Cyclic Di-GMP—Local Signaling in the Interactome of GGDEF/EAL Domain Proteins of Escherichia coli

Trigger phosphodiesterases as a novel class of c-di-GMP effector proteins

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