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Journal of Bacteriology, August 2000, p. 4425-4429, Vol. 182, No. 16
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
The Chromosomal Location of the Bacillus
subtilis Sporulation Gene spoIIR Is Important for
Its Function
Anastasia
Khvorova,
Vasant
K.
Chary,
David W.
Hilbert, and
Patrick J.
Piggot*
Department of Microbiology and Immunology,
Temple University School of Medicine, Philadelphia, Pennsylvania
19140
Received 16 March 2000/Accepted 25 May 2000
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ABSTRACT |
Formation of the asymmetrically located septum during sporulation
of Bacillus subtilis results in enclosure of the
origin-proximal 30% of the chromosome in the prespore compartment. The
rest of the chromosome is then translocated into the prespore from the mother cell. Transcription of spoIIR is initiated in the
prespore by RNA polymerase containing 
F soon after the
septum is formed. The SpoIIR protein is required for the activation of
the transcription program directed by E in the mother
cell. The spoIIR locus is located at 324°, near the
origin of replication (0/360°). We show here that movement of
spoIIR to 28° had little effect on sporulation. However,
movement to regions not in the origin-proximal part of the chromosome
substantially reduced sporulation efficiency. At 283° sporulation was
reduced to less than 20% of the level obtained when spoIIR
was at its natural location, and movement to 190° reduced sporulation
to about 6% of that level. These positional effects were also seen in
the transcription of a spoIIR-lacZ fusion. In contrast,
movement of other spo-lacZ fusions from 28° to 190° had
little effect on their expression. These results suggest that
spoIIR is the subject of "positional regulation," in
the sense that the chromosomal position of spoIIR is
important for its expression and function.
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INTRODUCTION |
During sporulation Bacillus
subtilis undergoes an asymmetrically located cell division. This
division is a modified form of the vegetative division (6,
16). However, formation of the sporulation septum results in
enclosure of only about 30% of a chromosome in the smaller cell, the
prespore (also called the forespore), that results from the division;
the rest of the chromosome is then translocated from the larger cell,
the mother cell, into the prespore by an active process requiring
SpoIIIE (Fig. 1) (23, 25). A
second copy of the chromosome remains in the mother cell. The prespores
of SpoIIIE mutant cells contain only about 30% of a chromosome, with
the other 70% remaining in the mother cell together with the whole of
the mother cell chromosome (23). Formation of the
asymmetrically located septum is followed by activation of two
sporulation-specific transcription factors, F in the
prespore and E in the mother cell, which specify
different programs of gene expression in the two compartments (reviewed
in reference 21). In a spoIIIE36 mutant
the F-directed prespore genes that are located in the
70% of the chromosome distal to the origin of replication (for
example, dacF and gpr) are not transcribed,
whereas those located in the origin-proximal 30% are transcribed (for
example, spoIIR and spoIIQ) (9, 12, 20, 22,
23, 25). Thus, it has been known for some time that chromosome
position is important for expression of F-directed genes
in a spoIIIE36 mutant (22). It seemed plausible that there could be some prespore-specific gene (or genes) that needed
to be expressed as soon as the septum was formed and so needed to be
located at the origin-proximal part of the chromosome in the parental,
spo+ strain. If such a gene were to be relocated
distal to the origin, its expression during sporulation might be
impaired, resulting in a sporulation-deficient phenotype.
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FIG. 1.
Model for chromosomal translocation through the
sporulation septum showing the approximate location of loci used in
this study (adapted from reference 24). The SpoIIIE
protein is indicated as ovals at the position where the chromosome
transverses the recently formed sporulation septum.
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We considered that the spoIIR locus might be a possible
candidate for this "positional" type of regulation of its activity. The spoIIR locus is near the origin and is transcribed only
by RNA polymerase containing F (9, 13). It
links the activation of E in the mother cell to the
activation of F in the prespore, and it is the only
F-directed gene needed for the E
activation (9, 13). Its activation is thought to ensure that
E is not activated until after the septum is formed
(9), and rapid activation of E following
septation may be important in preventing further septation (1). Thus, a delay in spoIIR expression may
disrupt the complex network of transcription regulation that is
necessary for spore formation. Below we describe experiments indicating
that the spoIIR gene is the subject of such positional regulation.
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MATERIALS AND METHODS |
Media.
B. subtilis was grown in modified Schaeffer's
sporulation medium (MSSM) and on Schaeffer's sporulation agar
(17, 19). When required,
5-bromo-4-chloro-3-indolyl-
-D-galactoside at 40 µg/ml,
chloramphenicol at 5 µg/ml, neomycin at 3 µg/ml, and erythromycin at 1 µg/ml were added.
Strains.
B. subtilis 168 strain BR151 trpC2
metB10 lys-3 and B. subtilis ZB307
SPc2
2::Tn917::pSK106 were used
as the parent strains. These and the other B. subtilis
strains used are listed in Table 1.
Escherichia coli strain DH5
(GIBCO/BRL) was used to
maintain plasmids.
The
spoIIR promoter region was cloned as a
NotI-
HindIII fragment (
9), via
pBluescript to provide additional sites, into
the following plasmids:
pMLK83, a
neo gusA fusion vector designed
for the
integration of constructs by a double-recombination event
at the
amyE locus (
10); pDG793, an
erm lacZ
fusion vector designed
for the integration of constructs by a
double-recombination event
at the
thrC locus (a gift from P. Stragier, Institut de Biologie
Physico Chimique, Paris, France); pGV34
(
4,
26), a
cat lacZ fusion vector designed for
the integration of constructs by a
double-recombination event at the
SP
locus, and also used for
Campbell-like recombination at
spoIIR. An intact copy of
spoIIR was cloned as a
1.2-kb
NotI-
XhoI fragment into the same plasmids.
The genetic linkage was verified for each chromosomal
insertion.
The
spoIIE promoter region was cloned as an
EcoRI-
PvuII fragment in pMLK83 (
10).
This construct was then used to introduce
the
spoIIE-gusA
fusion into
amyE by double crossover. The
spoIID-gusA fusion at
amyE was derived from
pMLK87 (
10). The
spoIID-lacZ fusion at
spoIID resulted from integration of pMLK23 by a single
crossover (
10). P. Youngman (Millennium Pharmaceuticals,
Cambridge,
Mass.) kindly provided strains containing the
spoIIE-lacZ and
spoIID-lacZ fusions at SP
. A
strain containing a
spoIIQ-gfp transcriptional
fusion
(
12) was kindly provided by P. Stragier. The fusion was
introduced by transformation into strains containing
spoIIR
at
different chromosomal locations. Details of the construction of
strains are available on
request.
-Galactosidase and -glucuronidase assays.
Assays were
performed essentially as described previously (10), using
lysozyme to permeabilize the cells. Specific activity (in units) is
expressed as nanomoles of
o-nitrophenyl--D-galactoside or
p-nitrophenyl--D-glucuronide hydrolyzed per
minute per milligram of bacterial dry weight. The endogenous
-galactosidase and -glucuronidase activities were determined in
each experiment for an isogenic parental strain lacking a fusion and
subtracted from the corresponding values for the fusion-containing strains.
Other methods.
B. subtilis transformation,
transduction, sporulation by exhaustion in MSSM, and all genetic
engineering methods were performed essentially as previously described
(7, 15, 17, 28). Sporulation was assayed 18 h after the
end of exponential growth by diluting cultures and determining the
heat-resistant count (80°C, 20 min) and the viable count in the
diluted cultures. The viable count varied somewhat from experiment to
experiment: for strains with spoIIR at SP, SL7256, and
SL7344, the range was 1.0 × 108 to 2.5 × 108 per ml; for all other strains the range was 2.5 × 108 to 6.0 × 108 per ml; there was no
significant chain formation.
Cultures used for visualization of green fluorescence protein (GFP)
were grown in MSSM at 33.5°C and harvested 6 h after the
end of
exponential growth, by which time the bulk of the population
had
reached the sporulation division stage. Culture samples of
10 µl of
unfixed cells were transferred to 0.1% polylysine-coated
slides
and examined by fluorescence microscopy essentially as
described
previously (
28).
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RESULTS |
Complementation of the Spo
phenotype associated with
spoIIR::neo by placing the intact
spoIIR gene at different chromosomal locations.
A
knockout of the spoIIR gene with an insertion of a
neo cassette in codon 98 of the spoIIR open
reading frame (9) resulted in an asporogenous phenotype
(less than 1 spore in 108 cells). To test the possibility
that the chromosomal location (at 324°) of the spoIIR gene
near the origin of replication (at 0/360°) might be important for its
proper functioning, we chose three different chromosomal locations
(11) for the integration of spoIIR: near the
origin but on the other side of the origin to spoIIR (at
amyE, 28°), approximately halfway from the origin to the
terminus (at thrC, 283°), and near the terminus (at SP, 190°). The intact copy of spoIIR as a
NotI-XhoI fragment was cloned in different
plasmids, pDH32, pDG793, and pGV34, designed to facilitate integration
of spoIIR by double crossover at amyE,
thrC, and SP, respectively. The results of sporulation
efficiency assays of strains carrying the knockout of spoIIR
at its original location (324°) and integration of an intact copy of
spoIIR at the different locations are summarized in Table
2. Movement of the intact copy of
spoIIR to amyE had little effect on sporulation.
However, movement to thrC reduced sporulation to less than
20% of the efficiency of the isogenic parent strain. Movement to SP
reduced sporulation to about 6% of that of the parent (Table 2); the
method of determining sporulation may overestimate this figure because
the viable counts of strains with spoIIR at SP were about
twofold lower than those of the other strains. The same effect of
movement to SP was also observed with a B. subtilis
strain of a different lineage, ZB307 (29). The results
suggest that the efficiency of sporulation depends on the distance
between the location of the spoIIR gene and the origin of
replication.
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TABLE 2.
Efficiency of sporulation of strains carrying a single
intact copy of spoIIR at different chromosomal locations
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Expression of a spoIIR-lacZ fusion in different
chromosomal locations.
To test spoIIR transcription at
the different locations, we employed a spoIIR-lacZ
transcriptional fusion in strains that also contained a
spoIIR-gusA fusion inserted at amyE as an
internal control. No significant differences were observed in the
timing or the level of expression of spoIIR-lacZ integrated
at spoIIR compared to the spoIIR-gusA fusion at
amyE (Fig. 2A). Expression of
spoIIR-lacZ was reduced at thrC (Fig. 2B) and was
barely detectable at SP (Fig. 2C). Introduction of an inducible copy
of the gene for F, spoIIAC, under the control
of the Pspac promoter (5) into the latter strain
established that the spoIIR-lacZ at SP fusion was still
functional (data not shown).
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FIG. 2.
Expression of spoIIR at various chromosomal
locations in a spoIIA+ background.  ,
expression of amyE::spoIIR-gusA.  ,
expression of spoIIR-lacZ at spoIIR (SL7205) (A),
thrC (SL7310) (B), or SP (SL7303) (C). SL7310 is a
derivative of BR151; SL7205 and SL7303 are derivatives of ZB307.
Gal, -galactosidase; Glu, -glucuronidase.
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We considered it unlikely that the local context of SP
would explain
the reduced expression of
spoIIR-lacZ. The SP
system
(
29) has been used extensively, and we had noted no
reduction
in expression of the strong
H promoter,
ftsAp2, when it was located at SP
(
3).
However,
we considered it necessary to retest the possibility that
expression
of
lacZ fusions at SP
might somehow be
inhibited by the local
gene context. We compared the expression at
amyE and SP
of the
A-dependent
sporulation-specific gene
spoIIE, which is also very
weakly
expressed. There was no difference in the level and pattern
of
expression, regardless of chromosomal position (Fig.
3). Fusions
to
gusA were used
at
amyE, and
lacZ fusions were used at SP
;
previous studies had shown that the
gusA and
lacZ
fusions gave
activities similar to each other (
10).
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FIG. 3.
Expression of spoIIE at different chromosomal
locations. , amyE::spoIIE-gusA; ,
SP::spoIIE-lacZ (SL7213). Gal,
-galactosidase; Glu, -glucuronidase.
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The transcription of
spoIIR is normally weak and is
substantially higher in
spoIIAC(P) mutants
(
9). Consequently we checked
spoIIR-lacZ
expression at the different locations in a
spoIIAC561 background in order to visualize more clearly possible
differences
in expression patterns. The
spoIIAC561 mutation
is a V233M change
in the 4.2 promoter recognition region of
F and does not affect regulation of
F
activity (
14,
27). It curtails transcription of some
F-directed genes (
14,
27) but enhances
transcription of
spoIIR (
9). Again, no
significant differences were observed in the
timing or level of
expression of
spoIIR-lacZ at
spoIIR compared
to
spoIIR-gusA at
amyE (Fig.
4). When the fusion was integrated
at
SP
, there was a delay in expression of
spoIIR-lacZ, and
expression
was also reduced compared to that of
spoIIR-gusA
at
amyE. The
delay was difficult to measure accurately; in
different experiments
it was about 15 to 20 min. These data indicate
that chromosome
position is important for the expression of
spoIIR; they suggest
that the SpoIIIE-mediated active
transport of the distal 70% of
the chromosome through the sporulation
septum into the prespore
(
25) may take 15 to 20 min.
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FIG. 4.
Expression of spoIIR at different chromosomal
locations in a spoIIA561 background. , expression of
amyE::spoIIR-gusA; , expression of
spoIIR-lacZ at spoIIR (SN178) (A) or SP
(SL7304) (B). Gal, -galactosidase; Glu, -glucuronidase.
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Activity of E is significantly decreased when the
spoIIR chromosomal location is altered.
Having the
level of spoIIR expression at SP significantly decreased
and delayed, it was reasonable to expect that expression of
E-dependent genes would be impaired. To test this
expectation, we introduced a spoIID-lacZ fusion into strain
ZB307 and into a derivative of ZB307 carrying a single functional copy
of the spoIIR gene at SP. The pattern of
spoIID-lacZ expression in cultures of these two strains is
shown in Fig. 5. Relocation of the
spoIIR gene to the terminus region resulted in reduction in
expression by about 80%, and this was accompanied by a delay compared
to spoIID-lacZ expression in the parent strain. It seems
plausible that the sporulation-deficient phenotype of strains
containing spoIIR located only at SP is the result of a
decrease in E-dependent gene expression.
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FIG. 5.
Effect of spoIIR location on expression of
spoIID-lacZ. , spoIIR at spoIIR
(SL7321); , spoIIR at SP (SL7322). Gal,
-galactosidase.
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The major role of
spoIIR is thought to be to ensure that
activation of
E requires prior activation of
F, and so
E activation follows formation
of the sporulation septum (
9).
Mutations in the structural
gene for
E,
spoIIGB, result in the abortively
disporic phenotype in which
a sporulation division has occurred near
both cell poles, and
it is inferred that a role of
E
during sporulation is to prevent the formation of the second,
asymmetrically located division septum (
1). Mutation of
spoIIR also results in this abortively disporic phenotype
(in which each
of the prespores contains a nucleoid, whereas the mother
cell
is nucleoid free), although at a slightly reduced frequency
(
9)
(our unpublished results). Appearance (or lack thereof)
of the
abortively disporic phenotype is used here as a separate test
of
the effect on
E activation of moving
spoIIR.
The prespore-specific expression
of a
spoIIQ-gfp
transcriptional fusion (
12) was used as an indicator
of
prespore formation. In this system, a
spoIIGB mutant gave
45%
disporic and 55% monosporic organisms displaying GFP fluorescence
6 h after the start of sporulation at 33.5°C. When an intact
copy
of
spoIIR was located at SP
, the strain exhibited an
abortively
disporic phenotype, similar to that of a
spoIIR
null mutant, with
about 30% of fluorescing organisms displaying the
disporic pattern
(Table
3); a similar
pattern was obtained for strains constructed
in the ZB307 background
(data not shown). Disporic forms were
very rare when
spoIIR
was located at
spoIIR or at
amyE (Table
3).
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TABLE 3.
Frequency of monosporic and disporic phenotypes in
strains having spoIIR at different
chromosomal locationsa
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DISCUSSION |
An early stage in sporulation of B. subtilis is an
asymmetric cell division that forms the prespore and the mother cell
(1, 16, 21). Shortly after the division, F
becomes active and governs gene expression in the prespore
(21). However, the asymmetrically located division septum,
when first formed, traps the origin-distal 70% of the
prespore-destined chromosome in the mother cell (25) (Fig.
1); movement of the rest of the chromosome into the prespore is an
active process requiring the membrane-associated DNA translocase
SpoIIIE (23). Thus, a F-dependent gene whose
activity is required early in the prespore may need to be located near
the chromosome origin. Our results demonstrate impaired sporulation
when the F-dependent spoIIR locus is moved
away from the origin to either the thrC locus (283°; less
than 20% of the sporulation of the isogenic parent with
spoIIR at its natural position) or SP (190°; about 6%)
(Table 2). This phenotype can be explained by the observed impairment
in spoIIR expression at the origin-distal locations. With a
spoIIAC561 background, which enhances spoIIR
transcription (9), we were able to observe that
spoIIR-lacZ expression was delayed when the fusion was
located at SP (Fig. 4). This delay is thought to represent the time
required for SpoIIIE-dependent chromosome translocation through the
sporulation septum. The 15- to 20-min estimate agrees with that of
Pogliano et al. (18) obtained from microscopy studies. These
observations are in agreement with the hypothesis that chromosome
partitioning during sporulation is an active, unidirectional, and
time-requiring process (23, 25). Frandsen et al.
(2) have utilized the transient gene asymmetry resulting
from this slow chromosome partitioning to engineer activation of
F independent of its normal regulators, SpoIIAA,
SpoIIAB, and SpoIIE.
Why may a delay in the prespore localization of the spoIIR
gene result in significantly lower expression? The native
spoIIR promoter is weak (9, 13). Thus, when
spoIIR is located near the terminus, one possibility is that
the observed decrease in its expression results from competition with
other F-directed genes that now precede
spoIIR into the prespore. In this regard, Ju et al.
(8) have shown that expression of another F-directed gene is higher when the gene is located
nearer to the origin. The role of SpoIIR in spore formation is to
activate E in the mother cell (9, 13), and a
consequence of E activation is to block further
septation (1). It is thought that spoIIR needs to
be expressed very soon after the septum is formed (9).
Reducing and/or delaying spoIIR expression is presumably sufficient to disrupt the delicate balance of controls that coordinate transcription between mother cell and prespore (21). The
positional type of transcription regulation for spoIIR may
thus be critical to the complex sporulation process.
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ACKNOWLEDGMENTS |
We thank W. Harling for help in an early part of the study. We
thank M. L. Karow, P. Stragier, and P. Youngman for plasmids and
strains used in this study. We are especially grateful to A. Wolfson
for many helpful discussions.
This work was supported by Public Health Service grant GM43577 from the
National Institutes of Health.
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FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology and Immunology, Temple University School of Medicine,
Philadelphia, PA 19140. Phone: (215) 707-7927. Fax: (215) 707-7788. E-mail: piggot{at}astro.ocis.temple.edu.
Present address: Department of Molecular, Cellular and
Developmental Biology, University of Colorado, Boulder, Colo.
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Journal of Bacteriology, August 2000, p. 4425-4429, Vol. 182, No. 16
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Abstract
Introduction
