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Dual-specificity anti-sigma factor reinforces control of cell-type specific gene expression in Bacillus subtilis.

Serrano M, Gao J, Bota J, Bate AR, Meisner J, Eichenberger P, Moran CP, Henriques AO - PLoS Genet. (2015)

Bottom Line: We also show that CsfB prevents activation of σG in the mother cell and the premature σG-dependent activation of σK.The capacity of CsfB to directly block σE activity may also explain how CsfB plays a role as one of the several mechanisms that prevent σE activation in the forespore.Thus the capacity of CsfB to differentiate between the highly similar σF/σG and σE/σK pairs allows it to rinforce the cell-type specificity of these sigma factors and the transition from early to late development in B. subtilis, and possibly in all sporeformers that encode a CsfB orthologue.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Estação Agronómica Nacional, Oeiras, Portugal.

ABSTRACT
Gene expression during spore development in Bacillus subtilis is controlled by cell type-specific RNA polymerase sigma factors. σFand σE control early stages of development in the forespore and the mother cell, respectively. When, at an intermediate stage in development, the mother cell engulfs the forespore, σF is replaced by σG and σE is replaced by σK. The anti-sigma factor CsfB is produced under the control of σF and binds to and inhibits the auto-regulatory σG, but not σF. A position in region 2.1, occupied by an asparagine in σG and by a glutamate in οF, is sufficient for CsfB discrimination of the two sigmas, and allows it to delay the early to late switch in forespore gene expression. We now show that following engulfment completion, csfB is switched on in the mother cell under the control of σK and that CsfB binds to and inhibits σE but not σK, possibly to facilitate the switch from early to late gene expression. We show that a position in region 2.3 occupied by a conserved asparagine in σE and by a conserved glutamate in σK suffices for discrimination by CsfB. We also show that CsfB prevents activation of σG in the mother cell and the premature σG-dependent activation of σK. Thus, CsfB establishes negative feedback loops that curtail the activity of σE and prevent the ectopic activation of σG in the mother cell. The capacity of CsfB to directly block σE activity may also explain how CsfB plays a role as one of the several mechanisms that prevent σE activation in the forespore. Thus the capacity of CsfB to differentiate between the highly similar σF/σG and σE/σK pairs allows it to rinforce the cell-type specificity of these sigma factors and the transition from early to late development in B. subtilis, and possibly in all sporeformers that encode a CsfB orthologue.

No MeSH data available.


Related in: MedlinePlus

The sporulation network and the action of CsfB on σG.A: the main morphological stages of sporulation are represented, with the main regulatory proteins active in the indicated cells. Pd, pre-divisional cell; Mc, mother cell; Fs, forespore; Sp, mature spore. B: organization of the transcriptional network of sporulation. The broken blue lines represent cell-cell signalling pathways. First, σF drives production of a protein, SpoIIR, secreted to the intermembrane space. SpoIIR then activates a membrane-embedded protease that triggers the proteolytic activation of pro-σE [18]. σE and σF activity are required for the assembly of a cell-cell secretion system (the SpoIIQ-SpoIIIAH channel in the figure) that, following engulfment completion, allows the mother cell to nourish the isolated forespore, thus enabling continued macromoelcualr synthesis and activation of the σG auto-regulatory loop [67]. Lastly, σG controls production of a signaling protein, SpoIVB, secreted into the intermembrane space that activates the machinery responsible for the proteolytical activation of σK [18]. The negative feedback loop through which σK limits production of σE is omitted for simplicity. C: the panel represents the composite negative feedback loop that operates in pre-divisional cells, and possibly also in the forespore prior to engulfment completion, to prevent activation of the σG positive auto-regulatory loop. Transcriptional and protein-protein interactions are shown in black and red, respectively. D: a single amino acid residue in region 2.1 (purple sector) allows CsfB to discriminate between the highly similar forespore sigma factors σF and σG: N45 of B. subtilis σG allows binding by CsfB, whereas a glutamate at the same position precludes binding. Conversely, a glutamate at the homologous position of σF (E39) impedes binding by CsfB whereas an asparagine at the same position is sufficient for binding. N45 and E39 are conserved among Bacillus orthologues of σG and σF.
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pgen.1005104.g001: The sporulation network and the action of CsfB on σG.A: the main morphological stages of sporulation are represented, with the main regulatory proteins active in the indicated cells. Pd, pre-divisional cell; Mc, mother cell; Fs, forespore; Sp, mature spore. B: organization of the transcriptional network of sporulation. The broken blue lines represent cell-cell signalling pathways. First, σF drives production of a protein, SpoIIR, secreted to the intermembrane space. SpoIIR then activates a membrane-embedded protease that triggers the proteolytic activation of pro-σE [18]. σE and σF activity are required for the assembly of a cell-cell secretion system (the SpoIIQ-SpoIIIAH channel in the figure) that, following engulfment completion, allows the mother cell to nourish the isolated forespore, thus enabling continued macromoelcualr synthesis and activation of the σG auto-regulatory loop [67]. Lastly, σG controls production of a signaling protein, SpoIVB, secreted into the intermembrane space that activates the machinery responsible for the proteolytical activation of σK [18]. The negative feedback loop through which σK limits production of σE is omitted for simplicity. C: the panel represents the composite negative feedback loop that operates in pre-divisional cells, and possibly also in the forespore prior to engulfment completion, to prevent activation of the σG positive auto-regulatory loop. Transcriptional and protein-protein interactions are shown in black and red, respectively. D: a single amino acid residue in region 2.1 (purple sector) allows CsfB to discriminate between the highly similar forespore sigma factors σF and σG: N45 of B. subtilis σG allows binding by CsfB, whereas a glutamate at the same position precludes binding. Conversely, a glutamate at the homologous position of σF (E39) impedes binding by CsfB whereas an asparagine at the same position is sufficient for binding. N45 and E39 are conserved among Bacillus orthologues of σG and σF.

Mentions: Spore formation in the bacterium Bacillus subtilis is an example of a prokaryotic cell differentiation process. At the onset of sporulation, triggered by severe nutrient scarcity, the rod-shaped cell divides close to one of its poles producing a small forespore, the future spore, and a larger mother cell (Fig. 1A). The mother cell nurtures development of the forespore, but undergoes autolysis to release the mature spore at the end of the process. Soon after asymmetric division, the mother cell engulfs the forespore, which becomes isolated from the external medium and separated from the mother cell cytoplasm by a double membrane and an intermembrane space. Following engulfment completion, gene expression in the mother cell drives the last stages of spore maturation by promoting the assembly of concentric protective structures. In parallel, gene expression in the forespore prepares the future spore for dormancy.


Dual-specificity anti-sigma factor reinforces control of cell-type specific gene expression in Bacillus subtilis.

Serrano M, Gao J, Bota J, Bate AR, Meisner J, Eichenberger P, Moran CP, Henriques AO - PLoS Genet. (2015)

The sporulation network and the action of CsfB on σG.A: the main morphological stages of sporulation are represented, with the main regulatory proteins active in the indicated cells. Pd, pre-divisional cell; Mc, mother cell; Fs, forespore; Sp, mature spore. B: organization of the transcriptional network of sporulation. The broken blue lines represent cell-cell signalling pathways. First, σF drives production of a protein, SpoIIR, secreted to the intermembrane space. SpoIIR then activates a membrane-embedded protease that triggers the proteolytic activation of pro-σE [18]. σE and σF activity are required for the assembly of a cell-cell secretion system (the SpoIIQ-SpoIIIAH channel in the figure) that, following engulfment completion, allows the mother cell to nourish the isolated forespore, thus enabling continued macromoelcualr synthesis and activation of the σG auto-regulatory loop [67]. Lastly, σG controls production of a signaling protein, SpoIVB, secreted into the intermembrane space that activates the machinery responsible for the proteolytical activation of σK [18]. The negative feedback loop through which σK limits production of σE is omitted for simplicity. C: the panel represents the composite negative feedback loop that operates in pre-divisional cells, and possibly also in the forespore prior to engulfment completion, to prevent activation of the σG positive auto-regulatory loop. Transcriptional and protein-protein interactions are shown in black and red, respectively. D: a single amino acid residue in region 2.1 (purple sector) allows CsfB to discriminate between the highly similar forespore sigma factors σF and σG: N45 of B. subtilis σG allows binding by CsfB, whereas a glutamate at the same position precludes binding. Conversely, a glutamate at the homologous position of σF (E39) impedes binding by CsfB whereas an asparagine at the same position is sufficient for binding. N45 and E39 are conserved among Bacillus orthologues of σG and σF.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4383634&req=5

pgen.1005104.g001: The sporulation network and the action of CsfB on σG.A: the main morphological stages of sporulation are represented, with the main regulatory proteins active in the indicated cells. Pd, pre-divisional cell; Mc, mother cell; Fs, forespore; Sp, mature spore. B: organization of the transcriptional network of sporulation. The broken blue lines represent cell-cell signalling pathways. First, σF drives production of a protein, SpoIIR, secreted to the intermembrane space. SpoIIR then activates a membrane-embedded protease that triggers the proteolytic activation of pro-σE [18]. σE and σF activity are required for the assembly of a cell-cell secretion system (the SpoIIQ-SpoIIIAH channel in the figure) that, following engulfment completion, allows the mother cell to nourish the isolated forespore, thus enabling continued macromoelcualr synthesis and activation of the σG auto-regulatory loop [67]. Lastly, σG controls production of a signaling protein, SpoIVB, secreted into the intermembrane space that activates the machinery responsible for the proteolytical activation of σK [18]. The negative feedback loop through which σK limits production of σE is omitted for simplicity. C: the panel represents the composite negative feedback loop that operates in pre-divisional cells, and possibly also in the forespore prior to engulfment completion, to prevent activation of the σG positive auto-regulatory loop. Transcriptional and protein-protein interactions are shown in black and red, respectively. D: a single amino acid residue in region 2.1 (purple sector) allows CsfB to discriminate between the highly similar forespore sigma factors σF and σG: N45 of B. subtilis σG allows binding by CsfB, whereas a glutamate at the same position precludes binding. Conversely, a glutamate at the homologous position of σF (E39) impedes binding by CsfB whereas an asparagine at the same position is sufficient for binding. N45 and E39 are conserved among Bacillus orthologues of σG and σF.
Mentions: Spore formation in the bacterium Bacillus subtilis is an example of a prokaryotic cell differentiation process. At the onset of sporulation, triggered by severe nutrient scarcity, the rod-shaped cell divides close to one of its poles producing a small forespore, the future spore, and a larger mother cell (Fig. 1A). The mother cell nurtures development of the forespore, but undergoes autolysis to release the mature spore at the end of the process. Soon after asymmetric division, the mother cell engulfs the forespore, which becomes isolated from the external medium and separated from the mother cell cytoplasm by a double membrane and an intermembrane space. Following engulfment completion, gene expression in the mother cell drives the last stages of spore maturation by promoting the assembly of concentric protective structures. In parallel, gene expression in the forespore prepares the future spore for dormancy.

Bottom Line: We also show that CsfB prevents activation of σG in the mother cell and the premature σG-dependent activation of σK.The capacity of CsfB to directly block σE activity may also explain how CsfB plays a role as one of the several mechanisms that prevent σE activation in the forespore.Thus the capacity of CsfB to differentiate between the highly similar σF/σG and σE/σK pairs allows it to rinforce the cell-type specificity of these sigma factors and the transition from early to late development in B. subtilis, and possibly in all sporeformers that encode a CsfB orthologue.

View Article: PubMed Central - PubMed

Affiliation: Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de Lisboa, Estação Agronómica Nacional, Oeiras, Portugal.

ABSTRACT
Gene expression during spore development in Bacillus subtilis is controlled by cell type-specific RNA polymerase sigma factors. σFand σE control early stages of development in the forespore and the mother cell, respectively. When, at an intermediate stage in development, the mother cell engulfs the forespore, σF is replaced by σG and σE is replaced by σK. The anti-sigma factor CsfB is produced under the control of σF and binds to and inhibits the auto-regulatory σG, but not σF. A position in region 2.1, occupied by an asparagine in σG and by a glutamate in οF, is sufficient for CsfB discrimination of the two sigmas, and allows it to delay the early to late switch in forespore gene expression. We now show that following engulfment completion, csfB is switched on in the mother cell under the control of σK and that CsfB binds to and inhibits σE but not σK, possibly to facilitate the switch from early to late gene expression. We show that a position in region 2.3 occupied by a conserved asparagine in σE and by a conserved glutamate in σK suffices for discrimination by CsfB. We also show that CsfB prevents activation of σG in the mother cell and the premature σG-dependent activation of σK. Thus, CsfB establishes negative feedback loops that curtail the activity of σE and prevent the ectopic activation of σG in the mother cell. The capacity of CsfB to directly block σE activity may also explain how CsfB plays a role as one of the several mechanisms that prevent σE activation in the forespore. Thus the capacity of CsfB to differentiate between the highly similar σF/σG and σE/σK pairs allows it to rinforce the cell-type specificity of these sigma factors and the transition from early to late development in B. subtilis, and possibly in all sporeformers that encode a CsfB orthologue.

No MeSH data available.


Related in: MedlinePlus