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Chapter 8 : Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System

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Abstract:

The initiation of sporulation in bacteria is a cellular response to deteriorating conditions for growth and division. Sporulation may be coupled to the cell cycle to suppress division and permit the orderly synthesis of spore membrane structural components in concert with chromosome replication. The nature of the integration mechanism for all this information is now becoming apparent, and its various regulatory features are discussed in this chapter. The two-component paradigm is at the heart of the signal transduction system, regulating the initiation of sporulation in sporulating bacteria. This system, the phosphorelay, differs from other two-component signal transduction systems by the mechanism of phosphate flow and types of accessory proteins that control phosphate flow in the system. The ultimate goal of the phosphorelay is to produce Spo0A~P, the activated form of this transcription factor that recognizes the 7-bp 0A box in sporulation promoters. Separate phosphatase proteins may only be necessary when two-component signal transduction systems are sensitive to multiple signal input, such as in sporulation, which may exhaust the signal recognition capacity of the kinase. The initiation of sporulation has adopted the two-component signal transduction system and made some unique modifications to adapt it to process multiple signal inputs. As more and more controls are discovered that act on the phosphorelay, it becomes even more amazing that sporulation occurs at all.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8

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Figures

Image of FIGURE 1
FIGURE 1

Phosphorelay signal transduction pathway of . The source of activated phosphate is either KinA or KinB, responding to signal A or signal B, respectively. The nature of the signals is unknown in both cases and, in the case of KinB, is thought to be transmitted through the cytoplasmic protein KapB. The flow of phosphate through the phosphorelay has the goal of producing Spo0A∼P, which is a transcription activator or repressor, recognizing the 7-bp sequence shown.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 2
FIGURE 2

Role of Spo0A∼P in transcription regulation of phosphorelay. The central goal of Spo0A∼P is depicted as either activation or repression of promoters. The small black boxes within the promoter show the location of 0A boxes. The + and - signs refer to the effect of Spo0A∼P on the 0A box. Promoters with more than one 0A box with opposite signs means Spo0A∼P is both an activator and a repressor of the promoter. Briefly, Spo0A∼P is an activator of σ promoters on the and genes and a repressor of the vegetative σ promoter on the gene and the gene. AbrB is a repressor of the transcription of the gene coding for σ. Spo0A∼P appears to play a role in the repression of the gene.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 3
FIGURE 3

Promoter switching at Spo0A promoter. The locations of the vegetative promoter P and the sporulation promoter P transcribed by σ and σ, respectively, are shown. The boxed nucleotides correspond to the 0A boxes, and the lines demarking both strands are the extent of coverage of each strand by the footprint analysis of Spo0A on this promoter. Note that the Spo0A boxes and positions of Spo0A binding occur between the P and the P promoters. Spo0A∼P is believed to bind preferentially at the top two 0A boxes, simultaneously accomplishing the repression of the P promoter and the activation of the P promoter. The Spo0A box located at about the -10 of the P promoter is believed to be a repression point where the P promoter is repressed when Spo0A∼P concentrations reach sufficiently high levels.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 4
FIGURE 4

Comparison of structural features of Spo0F and CheY. The structural features from the crystal structure of CheY of (A. ) and the structure of the Spo0F as determined by multidimensional nuclear magnetic resonance analyses (Feher, unpublished data) are presented. Wavy lines indicate regions of β-sheet, and black boxes indicate areas of β-helix.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 5
FIGURE 5

Kinase and phosphatase reactions on Spo0F. The kinases for sporulation are depicted as being activated by signal K, which either activates the autophosphorylation reaction of these kinases or converts the kinase to a phosphatase of Spo0F∼P. The actual mechanism of signal interpretation for either KinA or KinB on Spo0F has not been determined. Two phosphatases, RapA and RapB, are known to respond to different transcriptional activation signals, and presumably different effector molecules control their activity on Spo0F∼P. Sufficient Spo0F∼P for the production of Spo0A∼P only occurs in the absence of the activity of these (and perhaps other) phosphatases.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 6
FIGURE 6

Conversion of Spo0F∼P to Spo0A∼P. Spo0F∼P is a substrate for the Spo0B phosphotransferase, which transfers the phosphate group to Spo0A. Spo0A is depicted as inactive in the unphosphorylated state, and this probably occurs because the end-terminal 0A domain prevents access of the DNA binding domain to DNA. Phosphorylation of Spo0A causes a conformational change that exposes the DNA binding site, allowing this transcription factor to bind to 0A boxes in the promoters that it controls. The Spo0E protein is a phosphatase of activated Spo0A∼P and is thought to respond to some internal signal, signal E, of unknown nature.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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Image of FIGURE 7
FIGURE 7

Relationship between SinR and Spo0A∼P. SinR is a repressor of sporulation capable of binding to the promoters of several protease genes, as well as the promoters for the stage II genes, , , and . SinI is an inhibitor of the repressive functions of SinR, and this protein is produced at the end of exponential growth to relieve repression of sporulation. Transcription of SinI is activated by the accumulation of Spo0A∼P and inhibited by both Hpr and AbrB transition state regulators. Spo0A∼P is also a required activator for the transcription of the genes.

Citation: Hoch J. 1995. Control of Cellular Development in Sporulating Bacteria by the Phosphorelay Two-Component Signal Transduction System, p 129-144. In Hoch J, Silhavy T (ed), Two-Component Signal Transduction. ASM Press, Washington, DC. doi: 10.1128/9781555818319.ch8
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