Disappearance of the sigma E transcription factor from the forespore and the SpoIIE phosphatase from the mother cell contributes to establishment of cell-specific gene expression during sporulation in Bacillus subtilis.

ABSTRACT During the stage of engulfment in the Bacillus subtilisspore formation pathway, the larger mother cell engulfs the smaller forespore. We have tested the role of forespore-specific gene expression in engulfment using two separate approaches. First, using an assay that unambiguously detects sporangia that have completed engulfment, we found that a mutant lacking the only forespore-expressed engulfment protein identified thus far, SpoIIQ, is able to efficiently complete engulfment under certain sporulation conditions. However, we have found that the mutant is defective, under all conditions, in the expression of the late-forespore-specific transcription factor ςG; thus, SpoIIQ is essential for spore production. Second, to determine if engulfment could proceed in the absence of forespore-specific gene expression, we made use of a strain in which activation of the mother cell-specific sigma factor ςE was uncoupled from forespore-specific gene expression. Remarkably, engulfment occurred in the complete absence of ςF-directed gene expression under the same conditions permissive for engulfment in the absence of SpoIIQ. Our results demonstrate that forespore-specific gene expression is not essential for engulfment, suggesting that the machinery used to move the membranes around the forespore is within the mother cell.

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Establishment of Prespore-Specific Gene Expression inBacillus subtilis: Localization of SpoIIE Phosphatase and Initiation of Compartment-Specific Proteolysis

Journal of Bacteriology ◽

10.1128/jb.180.13.3276-3284.1998 ◽

1998 ◽

Vol 180 (13) ◽

pp. 3276-3284 ◽

Cited By ~ 13

Author(s):

Peter J. Lewis ◽

Ling Juan Wu ◽

Jeffery Errington

Keyword(s):

Gene Expression ◽

Bacillus Subtilis ◽

Sigma Factor ◽

Mother Cell ◽

Immunofluorescence Microscopy ◽

The Other ◽

Specific Gene ◽

Specific Gene Expression

ABSTRACT Immunofluorescence microscopy was used to study the establishment of compartment-specific transcription during sporulation inBacillus subtilis. Analysis of the distribution of the anti-anti-sigma factor, SpoIIAA, in a variety of mutant backgrounds supports a model in which the SpoIIE phosphatase, which activates SpoIIAA by dephosphorylation, is sequestered onto the prespore face of the asymmetric septum. Thus, prespore-specific gene expression apparently arises as a result of the compartmentalization of SpoIIE protein. The results also suggest the existence of at least two compartment-specific programs of proteolysis, one dependent on the mother cell-specific sigma factor ςE and the other dependent on the prespore-specific sigma factor ςF.

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Compartmentalization of Gene Expression during Bacillus subtilis Spore Formation

Microbiology and Molecular Biology Reviews ◽

10.1128/mmbr.68.2.234-262.2004 ◽

2004 ◽

Vol 68 (2) ◽

pp. 234-262 ◽

Cited By ~ 246

Author(s):

David W. Hilbert ◽

Patrick J. Piggot

Keyword(s):

Gene Expression ◽

Bacillus Subtilis ◽

Mother Cell ◽

Sigma Factors ◽

Specific Gene ◽

Subtilis Spore ◽

Insertion Element ◽

Specific Gene Expression ◽

Bacillus Subtilis Spore ◽

The Family

SUMMARY Gene expression in members of the family Bacillaceae becomes compartmentalized after the distinctive, asymmetrically located sporulation division. It involves complete compartmentalization of the activities of sporulation-specific sigma factors, σF in the prespore and then σE in the mother cell, and then later, following engulfment, σG in the prespore and then σK in the mother cell. The coupling of the activation of σF to septation and σG to engulfment is clear; the mechanisms are not. The σ factors provide the bare framework of compartment-specific gene expression. Within each σ regulon are several temporal classes of genes, and for key regulators, timing is critical. There are also complex intercompartmental regulatory signals. The determinants for σF regulation are assembled before septation, but activation follows septation. Reversal of the anti-σF activity of SpoIIAB is critical. Only the origin-proximal 30% of a chromosome is present in the prespore when first formed; it takes ≈15 min for the rest to be transferred. This transient genetic asymmetry is important for prespore-specific σF activation. Activation of σE requires σF activity and occurs by cleavage of a prosequence. It must occur rapidly to prevent the formation of a second septum. σG is formed only in the prespore. SpoIIAB can blockσ G activity, but SpoIIAB control does not explain why σG is activated only after engulfment. There is mother cell-specific excision of an insertion element in sigK and σE-directed transcription of sigK, which encodes pro-σK. Activation requires removal of the prosequence following aσ G-directed signal from the prespore.

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Analysis by fluorescence microscopy of the development of compartment-specific gene expression during sporulation of Bacillus subtilis.

Journal of Bacteriology ◽

10.1128/jb.176.10.2898-2905.1994 ◽

1994 ◽

Vol 176 (10) ◽

pp. 2898-2905 ◽

Cited By ~ 10

Author(s):

J E Bylund ◽

L Zhang ◽

M A Haines ◽

M L Higgins ◽

P J Piggot

Keyword(s):

Gene Expression ◽

Bacillus Subtilis ◽

Fluorescence Microscopy ◽

Specific Gene ◽

Specific Gene Expression

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The spoIIIA locus is not a major determinant of prespore-specific gene expression during sporulation in Bacillus subtilis.

Journal of Bacteriology ◽

10.1128/jb.172.12.6930-6936.1990 ◽

1990 ◽

Vol 172 (12) ◽

pp. 6930-6936 ◽

Cited By ~ 3

Author(s):

N Illing ◽

J Errington

Keyword(s):

Gene Expression ◽

Bacillus Subtilis ◽

Major Determinant ◽

Specific Gene ◽

Specific Gene Expression

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Contrasting Effects of σE on Compartmentalization of σF Activity during Sporulation of Bacillus subtilis

Journal of Bacteriology ◽

10.1128/jb.186.7.1983-1990.2004 ◽

2004 ◽

Vol 186 (7) ◽

pp. 1983-1990 ◽

Cited By ~ 10

Author(s):

David W. Hilbert ◽

Vasant K. Chary ◽

Patrick J. Piggot

Keyword(s):

Gene Expression ◽

Transcription Factor ◽

Bacillus Subtilis ◽

Mother Cell ◽

Cell Fates ◽

Gene Encoding ◽

Primitive Form ◽

Small Proteins ◽

Dna Translocase

ABSTRACT Spore formation by Bacillus subtilis is a primitive form of development. In response to nutrient starvation and high cell density, B. subtilis divides asymmetrically, resulting in two cells with different sizes and cell fates. Immediately after division, the transcription factor σF becomes active in the smaller prespore, which is followed by the activation of σE in the larger mother cell. In this report, we examine the role of the mother cell-specific transcription factor σE in maintaining the compartmentalization of gene expression during development. We have studied a strain with a deletion of the spoIIIE gene, encoding a DNA translocase, that exhibits uncompartmentalized σF activity. We have determined that the deletion of spoIIIE alone does not substantially impact compartmentalization, but in the spoIIIE mutant, the expression of putative peptidoglycan hydrolases under the control of σE in the mother cell destroys the integrity of the septum. As a consequence, small proteins can cross the septum, thereby abolishing compartmentalization. In addition, we have found that in a mutant with partially impaired control of σF, the activation of σE in the mother cell is important to prevent the activation of σF in this compartment. Therefore, the activity of σE can either maintain or abolish the compartmentalization of σF, depending upon the genetic makeup of the strain. We conclude that σE activity must be carefully regulated in order to maintain compartmentalization of gene expression during development.

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