Role of Cyclic Di-GMP in the Regulatory Networks of Escherichia coli

Regine Hengge

doi:10.1128/9781555816667.ch16

Chapter 16 : Role of Cyclic Di-GMP in the Regulatory Networks of Escherichia coli

Author: Regine Hengge¹

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Affiliations: 1: Institut für Biologie–Mikrobiologie, Freie Universität Berlin, 14195 Berlin, Germany

Content Type: Monograph

Publication Year: 2010

Category: Microbial Genetics and Molecular Biology

Book DOI: 10.1128/9781555816667

Chapter DOI: 10.1128/9781555816667.ch16

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Abstract:

This chapter provides an integrative picture that reflects general principles of cyclic di-GMP (c-di-GMP) signaling as well as specific molecular functions of the 29 GGDEF/EAL domain proteins of Escherichia coli and serves as a framework to elucidate the multiple functions of c-di-GMP signaling in a well-characterized model organism. E. coli is an environmentally versatile gram-negative bacterium that belongs to the gamma-proteobacteria and comes in a wide variety of strains that include commensals as well as important pathogens. The genomics era has revealed a striking abundance of genes encoding GGDEF and EAL domains in the genomes of many bacterial species (genes encoding HD-GYP domains are less frequent but can also be present several times in certain genomes). Functional sequestration and local operation of certain c-di-GMP control modules based on direct interactions in protein complexes can open new pathways for evolution. With a wealth of genome sequences now available, it has become apparent that c-di-GMP signaling indeed undergoes rapid evolution. Closely related species and even strains of the same species exhibit different sets of GGDEF/EAL domain proteins and use orthologs of these proteins in different regulatory circuits, suggesting that horizontal gene transfer and changes in regulation of expression are crucial for the rapid evolution of c-di-GMP signaling.

Citation: Hengge R. 2010. Role of Cyclic Di-GMP in the Regulatory Networks of Escherichia coli, p 230-252. In Wolfe A, Visick K (ed), The Second Messenger Cyclic Di-GMP. ASM Press, Washington, DC. doi: 10.1128/9781555816667.ch16

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Role of Cyclic Di-GMP in the Regulatory Networks of Escherichia coli

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Figure 1.

Growth phases and corresponding master regulators in E. coli K-12. In a culture of the E. coli K-12 strain W3110 growing in complex Luria-Bertani medium (LB), three growth phases can be distinguished: exponential or log phase (A), postexponential phase (B), and stationary phase (C). In the first part of the postex-ponential phase (starting at an optical density [OD] of approximately 0.3), the flagellar master regulator FlhDC and, therefore, flagella are expressed, but later on, further expression of FlhDC is shut down and existing FlhDC is degraded. As a consequence, further synthesis of flagella (and other proteins under FlhDC control) also comes to an end, but assembled flagella are active and cells are highly motile. In parallel, the master regulator of the stationary phase, σS, begins to accumulate but initially is only slowly assembling into active RNAP holoenzyme (Eσs). Upon entry into the stationary phase (at an OD of approximately 3), the regulator CsgD is induced, which is essential for the expression of adhesive curli fimbriae and other biofilm-related functions. Note that only relative amounts of the various regulatory proteins or complexes are shown, which cannot be compared directly. OD (578 nm), optical density of the culture measured at 578 nm; ON, overnight, i.e., at approximately 24 h. For further details and references, see the text.

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Figure 1.

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Figure 2.

Inverse coordination of motility and curli-mediated adhesion in E. coli K-12. The flagellar control cascade (FlhDC/FliA) interferes with the activity of the σS/CsgD/curli control cascade at two levels: (i) FliZ, which is expressed from a class 2 gene in the flagellar hierarchy, is an inhibitor of σ S activity at many σ S-dependent promoters, including those of ydaM, mlrA, and csgD; and (ii) the PDE YhjH, which is expressed from a class 3 gene (under σFliA control), degrades c-di-GMP and thereby keeps motility going while not allowing the activation of transcription of csgD and, therefore, curli expression. When the flagellar control cascade (including yhjH expression) shuts down in mid-postexponential phase, the DGCs YegE and YedQ, which are increasingly expressed due to the now accumulating σ S, outbalance the PDE activity of YhjH, and c-di-GMP can accumulate. Via YcgR, this c-di-GMP interferes with flagellar activity and, via an unknown effector, stimulates csgD transcription. In essence, this c-di-GMP control module acts as a checkpoint that allows curli expression only after flagellar gene expression has ceased. In parallel, a second DGC/PDE system, YdaM/YciR, is expressed under σ S control. The latter system exclusively acts on csgD transcription in a way which is not additive with the effect of the YegE/YhjH system (but both systems are essential for activation). Additional c-di-GMP control modules operate downstream of CsgD expression and affect the expression of the curli structural operon csgBAC and cellulose biosynthesis. In principle, the activity of all DGCs and PDEs (probably with the exception of YhjH, which basically consists of an EAL domain only) is likely to be modulated by additional unknown signals (lightning bolts) perceived by their N-terminal sensor domains. Note, only relevant genes or proteins under FlhDC and σS control are shown here; overall, FlhDC and σS activate more than 60 and approximately 500 genes, respectively. For further details and references, see the text. HBB, hook basal body.

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Figure 2.

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Figure 3.

The degenerate EAL protein YcgF is a blue light-modulated antirepressor and controls a small-protein and two-component network that modulates biofilm formation. By direct protein-protein interaction, blue light-irradiated YcgF (or excess nonirradiated YcgF) releases the MerR-like repressor YcgE from its operator site upstream of the ycgZ-ymgABC operon (also yliL and ynaK are derepressed, but there the mechanism has not yet been studied). All gene products of these target genes are small proteins (78 to 90 amino acids). YmgB (and YmgA and YcgZ, to minor extents) modulates the biofilm-associated functions indicated via the two-component phosphorelay system RcsC/RcsD/RcsB. The bdm gene also encodes a small protein of unknown molecular function (71 amino acids). In addition, ybgS (encoding a small protein of 121 amino acids) is also under control of the YcgF/YcgE/YmgB cascade (ybgS is not included in the figure, as the mechanism of this regulation has not yet been clarified). At the levels of protein activity as well as gene expression, this system integrates blue light, low temperature, starvation, and probably other stress signals and, therefore, seems important for E. coli in an extrahost and probably aquatic environment. For further details and references, see the text. Adapted from reference 130 with permission.

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Figure 3.

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Figure 4.

Model for the evolution of second messenger signaling as illustrated by systems operating in E. coli. The simplest and probably most ancient form of second messenger signaling is represented by the E. coli cAMP signaling system (A) ( 9 , 92 ). Here, only one second messenger-producing enzyme (the adenylate cyclase Cya), one second messenger-degrading enzyme (the cAMP PDE CpdA), and one effector component (the transcription factor CRP) control a variety of promoter regions that all feature similar cAMP-CRP binding sites. More complex systems that integrate many more signals use multiples of all the components involved, as illustrated by c-di-GMP signaling in the control of flagellar activity and csgD transcription (B). In this system, several DGCs generate c-di-GMP, which in turn serves at least two effector components, indicating that this c-di-GMP is freely diffusible ( 91 ). The multiplicity of DGC, PDEs, effectors, and targets also allows the evolution of locally acting systems, in which complexes consisting of a DGC, a PDE, and an effector highly specifically interact with distinct targets (C). An example seems to be the YdaM/YciR system which specifically regulates csgD transcription ( 91 , 137 ) (the tentative protein interactions indicated in the figure are based on unpublished in vivo and in vitro data by S. Lindenberg, H. Weber, and R. Hengge). Finally, the YcgF/YcgE system (which is a paralog of YciR/MlrA) is an example of a locally acting system in which c-di-GMP signaling has been lost and which relies entirely on protein-protein interactions ( 130 ) (D). Adenylate cyclases or DGCs are shown as light gray ovals; PDEs (or proteins derived thereof, such as YcgF) are shown as dark gray hexagons.

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Figure 4.

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Tables

Role of Cyclic Di-GMP in the Regulatory Networks of Escherichia coli

/content/10.1128/9781555816667.ch16.ch16tab01

Table 1

GGDEF/EAL genes in Escherichia coli and Salmonella enterica serovar Typhimurium a

Table 1

GGDEF/EAL genes in Escherichia coli and Salmonella enterica serovar Typhimurium a

/content/10.1128/9781555816667.ch16.ch16tab02

Table 2

Summary of sequence features and expression data of GGDEF/EAL genes in E. coli K-12 a

Table 2

Summary of sequence features and expression data of GGDEF/EAL genes in E. coli K-12 a