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Previous Article | Next Article 
Journal of Bacteriology, October 1999, p. 6171-6175, Vol. 181, No. 19
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
The "Pro" Sequence of the Sporulation-Specific
Transcription Factor E Directs It to the Mother Cell
Side of the Sporulation Septum
Jingliang
Ju and
W. G.
Haldenwang*
Department of Microbiology, University of
Texas Health Science Center at San Antonio, San Antonio, Texas
78284-7758
Received 26 April 1999/Accepted 6 July 1999
 |
ABSTRACT |
E, a mother cell-specific transcription factor of
sporulating Bacillus subtilis, is derived from an inactive
precursor protein (pro-E). Activation of
E occurs when a sporulation-specific protease (SpoIIGA)
cleaves 27 amino acids from the pro-E amino terminus.
This reaction is believed to take place at the mother cell-forespore
septum. Using a chimera of pro-E and green fluorescent
protein (GFP) to visualize the intracellular location of
pro-E by fluorescence microscopy, and lysozyme treatment
to separate the mother cell and forespore compartments, we determined
that the pro-E::GFP signal, localized to the
forespore septum prior to lysozyme treatment, is restricted to the
mother cell compartment after treatment. Thus,
pro-E::GFP had been sequestered to the mother
cell side of the septum. This segregation of pro-E::GFP,
and presumably pro-E, to the mother cell is likely to be
the reason why E activity is restricted to that compartment.
| |
TEXT |
At an early stage in endospore
formation, Bacillus subtilis portions itself into two
compartments of unequal size contained within a common cell wall. Each
of these compartments has a unique developmental fate. The smaller,
prespore compartment is engulfed by the larger, mother cell
compartment, which nurtures it during subsequent stages of development.
When the sporulation process is complete, the mother cell lyses and the
mature spore is freed into the environment. The individualized program
of gene expression for each of these compartments is controlled by the
sequential appearance of compartment-specific transcription factors:
E and then K in the mother cell and
F and then G in the forespore (reviewed
in reference 34). The first of the mother
cell-specific factors (E), as well as its
counterpart in the prespore (F), is synthesized at the
onset of sporulation, but neither E nor F
becomes active until after the septation event establishes the two
compartments (6, 10, 19, 21, 24, 25, 32, 35, 36, 37).
E and F are each silenced by distinct
mechanisms. F is held inactive in a complex with an
inhibitor (SpoIIAB), while E is synthesized as an
inactive proprotein (1, 5, 7, 8, 21, 22, 25, 31, 33).
F is freed from SpoIIAB by the action of a second
protein (SpoIIAA), which binds to SpoIIAB in lieu of F
(1, 5, 8). In the preseptal cell, SpoIIAA is phosphorylated and inactive (8, 9, 25). SpoIIAA remains inactive in the mother cell but is activated in the prespore by SpoIIE, a
membrane-bound phosphatase (2-4, 7). In contrast,
pro-E is activated when 27 amino acids are removed from
its amino terminus (21, 26). Pro-E processing
is catalyzed by the sporulation-specific protease SpoIIGA (15,
29). SpoIIGA, like pro-E, is present in the
preseptal cell but is inactive until the septum forms (28).
Pro-E and SpoIIGA localize to the septum (11, 13,
16, 17). Processing is initiated when SpoIIR, a
F-dependent gene product, traverses the septum and
triggers SpoIIGA to cleave the "pro" sequence from E
(14, 18, 23, 39).
The mechanisms by which E and F become
activated in only one of the two compartments have been the subject of
much speculation (1-3, 13, 14, 17, 24, 31, 39). Fusions of
the phosphatase (SpoIIE) that is responsible for F
activation and green fluorescent protein (GFP) localize to the forespore septum (3, 4, 7). Recently, Wu et al. reported that septum-bound SpoIIE-GFP is preferentially released into the forespore compartment following lysozyme treatment (38).
This was interpreted as evidence for sequestration of SpoIIE to the forespore face of the septum and provided a plausible explanation for
how the activation of F could be limited to the
forespore. The conclusion that SpoIIE is sequestered to the forespore
has been questioned by others, who argue that the larger volume of the
mother cell could reduce the intensity of the GFP signal, leading to
the impression of forespore localization even if similar amounts of
SpoIIE-GFP are released from both sides of the septum (20).
Although the interpretation of the SpoIIE-GFP result is controversial,
the technique of separating forespore from mother cell by lysozyme
treatment remains useful.
We previously used a fusion of the E pro sequence and
GFP to show that the pro sequence can tether proteins to the forespore septum (16, 17). In the present work, we employed the same fusion to determine whether protoplasting of these cells would reveal a
preferential localization of the SigE-GFP fusion to either mother cell
or forespore. The B. subtilis strain that we examined carries a sigE::gfp fusion in which the
coding element for 55 amino acids from the amino terminus of SigE is
joined to GFP and integrated into the B. subtilis chromosome
at sigE (i.e.,
PspoIIG::sigE55::gfp) (Table 1). Due to the integration event,
the strain expresses the fusion from the sigE promoter in
lieu of sigE. The strain also carries a null mutation in the
processing-essential spoIIAC gene
(spoIIAC::erm) so as to insure that the
pro sequence is not cleaved from GFP due to normal sporulation
processing (16). Without SpoIIAC or a source of intact
E, the strain is Spo
and does not proceed
past stage II of sporulation (i.e., the sporulation septum forms but
the forespore is not engulfed by the mother cell). Instead of prespore
engulfment, a second septum is laid down at the pole of the cell
opposite that at which the first septum appeared. This disporic
morphology, with two forespore compartments bracketing the former
mother cell, is characteristic of cells that lack E.
Figure 1A consists of micrographs of this
strain at the disporic stage. As we had previously observed (16,
17), the pro-E55::GFP protein
preferentially localizes to the two sporulation septa (Fig.
1A2). To determine whether this septum-bound material is
present on both sides of the septa, we treated samples of the culture
with lysozyme to protoplast the cells and partially separate the
compartments. When this was done, the GFP signal was seen to localize
exclusively to the membrane of the mother cell compartment (Table
2). This is evident in Fig. 1B, where the
GFP signal (Fig. 1B2) forms a ring around the central
mother cell compartments (Fig. 1B1), while the DAPI
(4',6-diamidino-2-phenylindole)-stained chromosomes are partitioned to
the forespore compartments that bracket them (Fig. 1B3).
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FIG. 1.
Localization of pro-E55::GFP in
sporulating B. subtilis. Stationary-phase B. subtilis cells were diluted 1/200 in DS medium and incubated for
12 h at 30°C, an interval in which wild-type B. subtilis reaches stage III to stage IV (15) and the
SigE
PspoIIG::sigE55::gfp
strain displays a disporic morphology. Samples were prepared to
maximize the GFP signal, as previously described (16);
stained with DAPI; and either directly examined by microscopy (A) or
treated on the slide with lysozyme (34) (4 mg/ml for 30 to
60 s) and then examined (B). The cells were visualized by
phase-contrast microscopy (A1 and B1) and by
fluorescence microscopy to visualize either the
pro-E::GFP fusion (A2 and
B2) or DAPI-stained DNA (A3 and
B3). The images in each series depict the same cells under
each of the viewing conditions.
|
|
As a test of whether the apparent sequestration of the GFP signal to
the mother cell is due to a directed localization of pro-E55::GFP to the mother cell side of the septum or is
an artifact arising from differences in the sizes of the two
compartments and the amount of GFP that could be trapped in each, we
repeated the experiment using a GFP fusion protein in which
gfp was joined to the amino terminus of a sigE
allele (sigE335) which lacks the first 15 amino acids of the
E pro sequence (27). Unlike the fusion
protein which carried the intact pro sequence, the GFP in B. subtilis expressing
PspoIIG::sigE335::gfp did not localize to the septum (Fig.
2A2) and was easily
discernible in both the mother cell and forespore compartments
following protoplasting (Fig. 2B2) (Table 2). Thus,
membrane tethering is required for mother cell localization.
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FIG. 2.
Localization of the
PspoIIG::sigE335::gfp
product in sporulating B. subtilis. B. subtilis SPF5
(PspoIIG::sigE335::gfp)
was grown and examined as described in the legend to Fig. 1. Cells were
untreated (A) or lysozyme treated (B) and viewed with phase-contrast
microscopy (A1 and B1) and with GFP-enhanced
(A2 and B2) or DAPI-enhanced (A3
and B3) fluorescence microscopy.
|
|
As a further test of our ability to visualize GFP in the forespore, we
placed the sigE55::gfp fusion under
control of the F-dependent dacF promoter
(36, 37). This construction does not make the strain
Spo. To give the cells the same terminal phenotype as the
strains we had used in the experiments illustrated by Fig. 1 and
2, we introduced a null allele of sigE
(sigE
84) into the strain (27). When the
sigE84
PdacF::sigE55::gfp
strain was examined, the GFP signal could be seen to preferentially
accumulate in the forespore compartments (Fig.
3). There was, however, a weaker but
discernible GFP signal in the mother cell (Table 2; Fig. 3A2 and B2). This is likely due to active
F in the mother cell compartment of this mutant strain.
The SpoIIE phosphatase, which activates F and which
normally disappears from the mother cell following septation, has been
shown to persist in the mother cell compartment if sporulation is
blocked due to the absence of E (30). Thus,
partial activation of F and limited expression of
dacF in this mutant's mother cell compartment would not be
unexpected. An additional feature of the GFP pattern is that one of the
forespore compartments typically gave a stronger signal than the other
(Fig. 3B2). Presumably, the stronger signal represents the
compartment that formed as a result of the first asymmetric division,
with the second appearing later and accumulating less GFP.
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FIG. 3.
Localization of the
PdacF::sigE55::gfp
product in sporulating B. subtilis. B. subtilis SFG7
(sigE84
PdacF::sigE55::gfp)
was grown and examined as described in the legend to Fig. 1. Cells were
untreated (A) or lysozyme treated (B) and viewed with phase-contrast
microscopy (A1 and B1) and GFP-enhanced
(A2 and B2) or DAPI-enhanced (A3
and B3) fluorescence microscopy.
|
|
Translocation of pro-E to the mother cell side of the
septum was proposed by Hofmeister as a plausible mechanism for its
mother cell specificity (13). Our present finding that the
fluorescent signal of pro-E::GFP, previously localized
at the forespore septum, becomes restricted to the mother cell
compartment following lysozyme treatment supports this model. The
conclusion that the GFP signal is localized to this compartment is not
subject to the criticism leveled at the apparent localization of
SpoIIE-GFP to the forespore (20). The mother cell is the
larger of the two compartments and, as such, is the compartment in
which the intensity of a GFP signal would be more likely to dissipate
when released from the septum (20). We conclude that the
E pro sequence not only targets E to the
sporulation septum but also allows E to be
preferentially sequestered to the mother cell side of the forespore
septum. In earlier studies (17), we found that SigE, but not
SigE-GFP, is preferentially degraded in the forespore compartment.
Based on that result, we suggested that E degradation
could be responsible for the absence of E activity in
the forespore (17). The present data argue that pro-E mobilization to the mother cell side of the septum
is likely to be the primary vehicle that places E
activity in the mother cell and that the degradation of
E in the forespore probably represents a secondary
device to destroy any E which might inadvertently form
in the forespore.
The ability of the SigE pro sequence to target pro-E to
the mother cell side of the septum is intriguing. The primary sequence of the pro region suggests that it has an alpha-helical structure with
hydrophobic and positively charged faces (27). In this regard, it resembles antimicrobial peptides that are believed to
associate with membrane phospholipids via their positively charged
faces (12). Presumably, such a structure would allow the pro
sequence to be targeted to cell membranes. Once membrane bound, more
specific amino acid residues might make contact with yet-to-be-defined
membrane proteins for sequestration to the developing septum. It is
interesting to note that treatment with lysozyme caused a dispersal of
pro-E55::GFP over the mother cell membrane (Fig.
1B2) from its previous location at the septal poles (Fig.
1A2). Apparently, an organizing element is lost when the
integrity of the peptidoglycan is degraded.
| |
ACKNOWLEDGMENTS |
This work was supported by NSF grant MCB-9727927.
We thank R. Losick for constructive criticism.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr., San Antonio, TX 78284-7758. Phone: (210) 567-3957. Fax: (210) 567-6612. E-mail: Haldenwang{at}UTHSCSA.edu.
| |
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Journal of Bacteriology, October 1999, p. 6171-6175, Vol. 181, No. 19
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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