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Chapter 7 : Regulation of the Initiation of Endospore Formation in

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Abstract:

Under certain environmental conditions, cells of the bacterium can initiate a developmental process leading to the formation of dormant endospores. Much of the work on sporulation in has focused on several key questions such as What are the environmental conditions that control sporulation? The authors describe some of the regulatory circuits that control the initiation of sporulation and the conditions that influence the activity of the regulatory factors. The responses of the gram-positive soil bacterium to changing nutrient conditions have been studied extensively. Regulatory mechanisms exist to help ensure that cells do not initiate sporulation unless it is likely that they will be able to complete the process successfully. and encode transcription factors that are required for the initiation of sporulation. Both and are required for asymmetric division and for transcription of the genes required for establishing cell-type-specific gene expression. The genes controlled by Spo0A that are involved in formation of the axial filament and the polar FtsZ rings are not known. Extracellular and intracellular signals are generated by nutrient deprivation, cell density, DNA replication, DNA damage, glucose metabolism, the tricarboxylic acid (TCA) cycle, and chromosome-partitioning proteins. Understanding both the signals that regulate these pathways and the organization of the pathways into networks regulating gene expression will contribute significantly to an integrated view of the interplay among cell physiology, gene expression, adaptation, and development.

Citation: Burkholder W, Grossman A. 2000. Regulation of the Initiation of Endospore Formation in , p 151-166. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch7
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Image of FIGURE 1
FIGURE 1

Cell division cycle during vegetative growth and sporulation. During the vegetative cell cycle, cells grow along their long axes to roughly twice their length at birth and divide at midcell. Sporulating cells switch the site of septation to a polar site, so that septation yields a large and a small cell, the mother cell and the forespore, respectively. The nascent division site is marked in both vegetatively growing and sporulating cells by rings of FtsZ, a tubulin-like protein required for cytokinesis. Rings of FtsZ assemble near both cell poles in sporulating cells, but polar septation occurs at only one of the polar rings. The forespore subsequendy develops into a mature spore in a defined series of morphological stages (not shown), aided by the mother cell and culminating in lysis of the mother cell and release of the mature spore. Cells are proficient in making the transition from vegetative growth to the sporulation pathway only during a limited period of the cell cycle following replication initiation; this period probably ends when the cells become committed to another round of the vegetative cell cycle. The nucleoid mass, containing chromosomal DNA, is depicted in light gray, rings of FtsZ are depicted as thin black ovals, the polar septum at stage II of sporulation is depicted as a straight black line, and the mature spore coat is depicted as a thick black oval.

Citation: Burkholder W, Grossman A. 2000. Regulation of the Initiation of Endospore Formation in , p 151-166. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch7
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Image of FIGURE 2
FIGURE 2

The phosphorelay and production of Spo0A∼P. The sensor kinases KinA, KinB, and KinC autophosphorylate on a histidine. Phosphate is transferred to Spo0F, then to Spo0B, and finally to Spo0A. Low levels of Spo0A∼P are sufficient to repress transcription of , derepressing expression of many of the stationary-phase response pathways negatively regulated by AbrB. Higher levels of Spo0A∼P stimulate axial-filament formation, polar septation, and transcription of genes (e.g., and ) required for cell-type-specific gene expression.

Citation: Burkholder W, Grossman A. 2000. Regulation of the Initiation of Endospore Formation in , p 151-166. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch7
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Image of FIGURE 3
FIGURE 3

Positive and negative autoregulatory loops involved in production of Spo0A∼P. (A) is expressed from two promoters, a vegetative-growth-specific promoter, Pv, transcribed by sigma-A-as-sociated RNA polymerase holoen-zyme (EσA), and a sporulation-specific promoter, Ps, transcribed by sigma-H-associated RNA polymerase holoenzyme (EσH). Spo0A∼P can negatively autoregulate transcription by binding and inhibiting expression from Pv. Transcription from Ps is activated direcdy by Spo0A∼P and by the induction of sigma-H following starvation. (B) Spo0A∼P positively and negatively regulates its expression and activity by controlling the expression or activity of two other proteins, SinR and Spo0E. In a positive feedback loop stimulating transcription, Spo0A∼P inhibits the activity of a transcriptional repressor of , SinR, by inducing expression of a SinR inhibitor, Sinl. Spo0A∼P stimulates transcription of sinl by inhibiting expression of AbrB, a transcriptional repressor of both and the gene encoding sigma-H, , which drives transcription of sinl. Spo0A∼P also binds to the promoter region and direcdy activates transcription of . In a negative feedback loop inhibiting Spo0A activity, Spo0A∼P induces the expression of the phosphatase SpoOE, which specifically dephosphorylates Spo0A∼P. Spo0A∼P induces transcription ofspo0E by inhibiting expression of AbrB, which represses transcription. Arrows indicate activation; barred lines indicate inhibition.

Citation: Burkholder W, Grossman A. 2000. Regulation of the Initiation of Endospore Formation in , p 151-166. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch7
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Image of FIGURE 4
FIGURE 4

Sigma-H is required for the full expression and activation of Spo0A. Sigma-H drives transcription of kinA, , and , contributing to the accumulation of high levels of Spo0A∼P. Sigma-H also stimulates transcription of by driving expression of sinI, activating by inhibiting the activity of a transcriptional repressor, SinR. Sigma-H stimulates the activation of Spo0A by driving expression of the secreted peptide pheromone, CSF, which inhibits the phosphatase, RapB, that dephos-phorylates Spo0F∼P. Spo0A∼P contributes to the full induction of sigma-H by inhibiting AbrB, which inhibits transcription of spo0H, encoding sigma-H. Spo0A∼P also binds and stimulates transcription from the sigma-H-dependent promoters of and . Consequendy, all of the pathways shown here constitute positive feedback loops contributing to the high-level expression and activation of Spo0A. The arrows indicate activation; the barred lines indicate inhibition.

Citation: Burkholder W, Grossman A. 2000. Regulation of the Initiation of Endospore Formation in , p 151-166. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch7
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Image of FIGURE 5
FIGURE 5

Histidine protein kinases that donate phosphate to Spo0F. KinA is a cytosolic protein, and KinB and KinC are both integral membrane proteins. When activated, the kinases autophosphorylate and donate phosphate to Spo0F. Phosphate is then transferred to Spo0B and finally to Spo0A ( Fig. 2 ). KinA activity is inhibited (barred lines) by KipI and activated by KipA, which inhibits KipI. KinB activity requires several additional proteins, including the integral membrane protein KbaA and the extracytoplasmic lipoprotein KapB. Though KinB, KbaA, and KapB are depicted here in a complex, it has not yet been demonstrated that they interact directly. The heavy black Une represents the cell membrane.

Citation: Burkholder W, Grossman A. 2000. Regulation of the Initiation of Endospore Formation in , p 151-166. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch7
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Image of FIGURE 6
FIGURE 6

Cell density and cell cycle control of the phosphorelay. The physiological function of the phosphorelay is to integrate multiple signals that regulate sporulation. The secreted cell density peptides PhrA and CSF regulate the phosphorelay by inhibiting the activity of the RapA and RapB phosphatases, which negatively regulate Spo0F. Inhibiting the initiation of DNA replication or inducing the SOS response, which is induced by DNA damage, inhibits the activation of Spo0A. Genetic data indicate that either Spo0F or Spo0B, rather than the histidine kinases or Spo0A itself, is the likely target of this regulation ( ). The inhibition of sporulation that results from inhibiting the initiation of DNA replication is mediated by a signaling pathway independent of the SOS response. During the SOS response, RecA is activated and then causes inactivation of the transcriptional repressor DinR (LexA), causing induction of genes in the SOS regulon. At least one gene in the SOS regulon is postulated to be a negative regulator of the phosphorelay. Soj is a negative regulator of sporulation gene expression. Repression by Soj is antagonized by Spo0J, a protein required for accurate chromosome partitioning. The arrows (→) indicate activation; the barred lines (-1) indicate inhibition.

Citation: Burkholder W, Grossman A. 2000. Regulation of the Initiation of Endospore Formation in , p 151-166. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch7
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