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Chapter 15 : The General Stress Response in Gram-Negative Bacteria

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Abstract:

Being exposed to various kinds of stress in their natural environments, bacteria usually grow slowly or even have to use their limited resources entirely for maintenance and stress survival. The latter requires the induction of the general stress response, which, in and related gram-negative bacteria, depends on the σ (RpoS) subunit of RNA polymerase. σ is closely related to the vegetative sigma factor σ (RpoD) and these two sigma factors recognize similar but not identical promoter sequences. Target gene products have a variety of stress-protective functions that redirect metabolism, affect cell envelope and shape, are involved in biofilm formation or pathogenesis, or increase stationary phase and stress-induced mutagenesis. This chapter summarizes the diverse functions and the amazingly complex regulation of σ. At the molecular level, these processes are integrated with the partitioning of global transcription space by sigma factor competition for RNA polymerase (RNAP) core enzyme and signaling by nucleotide second messengers that include cAMP, (p)ppGpp, and c-di-GMP. Physiologically, σ is the key player in the balance between a lifestyle associated with slow growth based on nutrient scavenging and motility and a lifestyle focused on maintenance and strong stress resistance that can include a sedentary multicellular existence in a biofilm. The primary requirement for inducing the general stress response in is σ accumulation, with expression patterns of many σ-dependent genes then being fine-tuned by additional signal input.

Citation: Hengge R. 2011. The General Stress Response in Gram-Negative Bacteria, p 251-289. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch15

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Figures

Image of Figure 1.
Figure 1.

Growth phases and corresponding master regulators in K-12. With the K-12 strain W3110 growing in complex Luria-Bertani medium (LB), three growth phases are shown: (I) exponential or “log” phase, (II) postexponential phase, and (III) stationary phase. In the first part of the postexponential phase (starting at an OD of approximately 0.3), the flagellar master regulator FlhDC, the flagellar sigma factor σ or σ), and therefore flagella are expressed, but later on further expression of FlhDC is shut down and existing FlhDC is degraded. As a consequence, the expression of σ (and other proteins under FlhDC control) ceases, excess σ (not bound by its anti-sigma FlgM) is degraded, and further synthesis of flagella comes to an end. However, assembled flagella are active and cells are highly motile. In parallel, the master regulator of the stationary phase, σ, begins to accumulate, but initially is only inefficiently assembling into active RNAP holoenzyme (Eσ). During transition into stationary phase, Eσdependent gene expression is strongly stimulated. Note that only relative amounts of the various regulatory proteins or complexes that cannot be compared directly are indicated. The dynamics of the total cellular levels of σ and σ was measured by Lange and Hengge-Aronis ( ) and Barembruch and Hengge ( ), respectively. The relative amounts of active regulators (FlhDC, Eσ, and Eσ) reflect an average of the expression patterns of many of their respective direct target genes. OD(578 nm), optical density of the culture measured at 578 nm; ON, overnight (i.e., approximately 24 h). For further details and references, see main text. This figure is a modified version of a figure published in Hengge ( ) that is used here with permission.

Citation: Hengge R. 2011. The General Stress Response in Gram-Negative Bacteria, p 251-289. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch15
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Image of Figure 2.
Figure 2.

Signal input and phenotypic output of the general stress response. Stress conditions that result in cellular σ accumulation and phenotypic alterations induced by high σ levels are depicted.

Citation: Hengge R. 2011. The General Stress Response in Gram-Negative Bacteria, p 251-289. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch15
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Image of Figure 3.
Figure 3.

Figure 3. Diverse stress conditions affect different levels of σ control. Regulation of σ occurs at the levels of transcription, translation, proteolysis, and association with RNAP core enzyme. Stress conditions affecting this regulation are indicated as well as regulatory proteins, small RNAs, and second messengers that participate in the underlying regulatory mechanisms (see text for details).

Citation: Hengge R. 2011. The General Stress Response in Gram-Negative Bacteria, p 251-289. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch15
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Image of Figure 4.
Figure 4.

Molecular mechanisms in the regulation of σ. In particular detail, the homeostatic σ/RssB/σ feedback cycle is shown and several competition, titration, and sequestration mechanisms that integrate numerous stress signals in the control of RssB/ClpXP-mediated σ proteolysis. Key features are the maintenance of a distinct σ:RssB ratio by the homeostatic feedback loop (up to a certain threshold where the promoter is saturated by Eσ) and the competition of RssB and RNAP core enzyme (E) for σ. For the detailed functions of all components and the regulatory consequences, see main text. This figure is a modified version of a figure originally published in (Jenal and Hengge-Aronis, ) that is used here with permission.

Citation: Hengge R. 2011. The General Stress Response in Gram-Negative Bacteria, p 251-289. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch15
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Image of Figure 5.
Figure 5.

Inverse coordination of the motile and adhesive lifestyles in K-12. This coordination is part of the more general transition from the foraging lifestyle of postexponentially, and therefore slowly growing, cells (with cAMP-CRP and Eσ acting as master regulators; phase II in Fig. 1 ) to the stationary phase lifestyle characterized by maintenance metabolism, stress resistance, high cell density, and cellular adherence (where Eσ acts as a master regulator; phase III in Fig. 1 ). The flagellar control cascade (FlhDC/FliA) interferes with the activity of the σ/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 activity at many σ-dependent promoters, including those of and ; and (ii) the PDE YhjH, which is expressed from a class 3 gene (under σ control), degrades c-di-GMP and thereby keeps motility going, while not allowing the activation of transcription of and therefore curli expression. When the flagellar control cascade (including expression) shuts down in mid-postexponential phase, the DGCs YegE and YedQ, which are increasingly expressed due to now accumulating σ, 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 transcription. In essence, this c-di-GMP control module acts as a checkpoint that allows curli expression only flagellar gene expression has ceased. In parallel, a second DGC/PDE system, YdaM/YciR, is expressed under σ control. The latter system exclusively acts on transcription in a way that is not additive with the effect of the YegE/YhjH system (but both systems are essential for activation). An additional c-di-GMP control module operates downstream of CsgD expression and affects the expression of cellulose biosynthesis. 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 (bolts) perceived by their N-terminal sensor domains. Note that only relevant genes or proteins under FlhDC and σ control are shown here; overall, FlhDC and σ activate more than 60 and 500 genes, respectively. For further details and references, see main text. This figure has been published previously (Hengge, ) and is used here with permission.

Citation: Hengge R. 2011. The General Stress Response in Gram-Negative Bacteria, p 251-289. In Storz G, Hengge R (ed), Bacterial Stress Responses, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816841.ch15
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