Department of Microbiology, University of
Connecticut Health Center, Farmington, Connecticut 06030
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INTRODUCTION |
The process of cytokinesis in
Escherichia coli and most other bacteria leads to formation
of two identical daughter cells that each contain a fully replicated
chromosomal complement. This process proceeds with high fidelity, so
that cytokinesis is restricted to the proper site at midcell and occurs
at the correct time in the cell cycle. In recent years, significant
advances have been made in understanding the assembly of the components
of the septal machinery (18). However, little is known about
how the position of the division site is determined.
Two general models have been proposed to explain how the position of
the division site is established. In the nucleoid occlusion model
(15, 23), the site of septum formation is determined solely
by the position of the nucleoids. According to this model, all
positions along the length of the cell are competent to support septation. However, an inhibitory influence from the nucleoid prevents
septation along most of the cell surface until segregation of the
daughter chromosomes occurs. When the chromosomes move apart, the
inhibitory effect would be gone at the middle of the cell, permitting
septation to occur at midcell. In addition, it has been suggested that
an activator of septation may be released upon termination of
chromosome replication to provide both temporal and spatial control of
septum formation (11, 15). Septation would occur at the
position where the action of the activator overcame the inhibitory
action of the nucleoid. The mechanism of site selection in bacteria
would therefore bear some resemblance to division site selection in
eucaryotes, where the location of the division site is markedly
affected by the position of the mitotic spindle and chromosome
segregation apparatus.
In the predetermined site model, the position of the division site is
established by a mechanism that is independent of nucleoid position,
and the future septation site can be identified and begin its
differentiation before the time of chromosome segregation. This model
is consistent with studies showing that FtsZ and ZipA rings are present
at midcell early in the division cycle and are sometimes also present
at the cell quarters (1, 8, 17). Similarly, the localized
plasmolysis bays that act as landmarks for periseptal annuli are
present at future division sites before chromosome segregation or
septal invagination occurs and are present at cell quarters in
predivisional cells (3).
We have used the following strategy to discriminate between the models.
Strains were constructed in which a long nucleoid-free region was
formed between the nucleoid and the cell pole. This was accomplished by
using mutants in which chromosome replication and cell division were
both inhibited. When the cell division block was released, septation
occurred within the nucleoid-free zone. This permitted us to ask
whether the positions of the division sites correlated with the
position of the nearest nucleoid, as predicted by the nucleoid
occlusion model, or whether the positions of the division sites were
independent of nucleoid position, as predicted from the predetermined
site model.
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MATERIALS AND METHODS |
Strains.
Strain details are summarized in Table
1. Strain WC1010 was constructed by
P1-mediated transduction of zic501::Tn10 from JW355 into PC5. WC1013 was constructed by P1-mediated cotransduction of
zic501::Tn10 and dnaA5(Ts)
from WC1010 into PB103 (7). WC1016 was constructed by
P1-mediated cotransduction of
zic501::Tn10 and dnaA5(Ts) from
WC1013 into WC1004, with selection for tetracycline-resistant colonies. The presence of the dnaA(Ts) allele was confirmed
by demonstrating the presence of clustered nucleoids and long anucleate regions in filaments that were formed during growth at 42°C. Cells of
WC1013 grown at 42°C did not form the long filaments seen in cultures
of WC1004 and WC1016.
WC1097(
GL100) was constructed by P1-mediated cotransduction of
zjb504::Tn10 and dnaB252(Ts) into
WC1092(GL100), a leu+, tetracycline-sensitive
derivative of WX7(GL100). GL100 and WX7(GL100) were
constructed by J. García-Lara in this laboratory. The presence of the dnaB(Ts) mutation in
WC1097(GL100) was confirmed by DAPI
(4',6-diamidino-2-phenylindole) staining as described above for
WC1016. WC1113(GL100) was constructed by P1-mediated transduction of
sfiA::Tn5 from GC4540 into
WC1097(GL100), selecting for kanamycin resistance.
Growth conditions.
For experiments with WC1016 (ftsA12
dnaA5), cells were grown at 30°C in high-salt medium (3×
concentrated M9 basal salts medium supplemented with 0.2% glucose and
1% Bacto Tryptone). This gave a doubling time of approximately 105 min. Overnight cultures were diluted into fresh medium, and
exponentially growing cells were collected by centrifugation and
suspended to an A600 of 0.05 in low-salt medium
(1/5 concentrated M9 basal salts medium containing 1.6% glucose and
1% Bacto Tryptone) prewarmed to 42°C; low-salt medium was used to
potentiate the division inhibition that occurs when ftsA12
cells are grown at a nonpermissive temperature. The culture was grown
at 42°C with shaking for a total of three doubling periods (120 min).
The culture was then diluted with an equal volume of
5.8-fold-concentrated M9 medium containing 1% Bacto Tryptone at room
temperature and shifted back to the 30°C shaking water bath for a
period of 100 min.
For experiments with WC1113(GL100), cells were grown in
Luria-Bertani (LB) broth containing
isopropyl-
-D-thiogalactopyranoside (IPTG [300 µM])
at 30°C. Cells from exponentially growing cultures were collected by
centrifugation, suspended to an A600 of 0.05 in
LB broth supplemented with 2.5% glucose, and returned to the 30°C
shaking water bath for 1 doubling period (85 min) to begin depletion of
cellular FtsZ. The culture was then transferred to a 42°C shaking
water bath for three doubling periods (78 min). Cells were collected by
centrifugation and suspended in 1 volume of LB broth (prewarmed to
42°C) containing 600 µM IPTG and then were returned to the 42°C
shaking water bath for a period of 30 min.
Microscopy.
Unless otherwise noted, 10-ml samples were
removed from the culture and fixed by the addition of glutaraldehyde
(2.3% final concentration). After 1 h at 4°C, the samples were
centrifuged (2,800 × g, 5 min, 4°C), and the pellets
were washed twice with 1 ml of phosphate-buffered saline (PBS) at 4°C
and then suspended in 1 ml of PBS. DAPI was added at approximately 0.5 µg per 109 cells. Fixation with osmium tetroxide was
performed by adding OsO4 (0.1% final concentration) to the
samples in place of glutaraldehyde. For OsO4-fixed cells,
DAPI was added to 5.0 µg per 109 cells in order to obtain
good staining.
Samples were then examined by Nomarski and fluorescence microscopy
(DAPI filter) and photographed with a charge-coupled device camera.
Measurements and analysis of cell lengths and positions of septa and
nucleoids were performed by using Optimas image analysis software as
described previously (4). Nucleoid-to-pole and nucleoid-to-septum distances were measured from the edge of the nucleoid that was nearest to the pole, unless otherwise noted. The
experimental reproducibility of measurements was ±0.06 µm (95%
confidence limits).
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RESULTS |
Septum placement in nucleoid-free regions of FtsA
DnaA filaments.
Strain WC1016 [dnaA5(Ts)
ftsA12(Ts)] was grown for three generations at 42°C.
Under these conditions, cell division was prevented because of the
ftsA(Ts) mutation, leading to formation of nonseptate filaments. At the same time, ongoing rounds of chromosome replication were completed, but new rounds were not initiated because of the dnaA(Ts) mutation. As a result, the population consisted of
long filaments in which one or more nucleoids were present in the
interior of the filaments, and there were extended chromosome-free
regions at the ends of the cells (Fig.
1A). The filaments differed from those of
the ftsA(Ts) parent, in which chromosome replication was not
inhibited and multiple nucleoids were distributed at regular intervals
along the entire length of the filaments (Fig. 1B). The filaments also
differed from those of the dnaA single mutant, in which long
filaments were not formed because of residual divisions that produced
anucleate cells (data not shown). It has previously been shown that
division continues in dnaA mutants because of failure to
induce the SOS response (12).
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FIG. 1.
Comparison of ends of ftsA(Ts)
dnaA(Ts) (A) and ftsA(Ts) (B) DAPI-stained
filaments from strains WC1016 and WC1004 after growth at 42°C for
three generations. (C) Cells of strain WC1016 were grown at 42°C for
three generations and then shifted to 30°C for 100 min as described
in Materials and Methods. The upper panel of each pair is the
fluorescence micrograph, and the lower panel is the corresponding
Nomarski image. Representative cells are shown. Arrowheads indicate
septa. Scale bar, 5 µm.
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When the ftsA(Ts) dnaA(Ts) double mutant was
shifted back to 30°C after three generations of growth under
nonpermissive conditions, septa began to form after approximately one
generation, reflecting the restoration of FtsA activity. Septa were
formed in the nucleoid-free regions at the cell poles (Fig. 1C) and
elsewhere along the length of the filaments. In some cells, a new
septum was formed directly over a nucleoid (discussed below). In the
present study, we restricted the analysis to septation that occurred
within the anucleate regions at the ends of the cells, since these
provided the longest available nucleoid-free regions. The micrographs
suggested that the septa were generally located at a similar distance
from the cell pole, whereas there was a considerable variation in
the distance from nucleoid to septum.
To confirm this impression and to determine whether nucleoid position
played a role in division site selection, the positions of all
septa located in the nucleoid-free regions that lay between the
cell pole and the nucleoid were analyzed. The average filament length was 50.1 µm (range of 20 to 117 µm), with nucleoid-to-pole distances varying between 4 and 42 µm (Fig.
2C). As shown in Fig. 2B, septa were not randomly distributed, but were predominantly located approximately 5.0 µm from the end of the cell. As shown in
Fig. 2D, the septum-to-pole distance was relatively constant and was
unrelated to the septum-to-nucleoid distance, which varied over a
wide range.
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FIG. 2.
Positions of septa and nucleoids at ends of
ftsA(Ts) dnaA(Ts) filaments. (A) Diagram showing
landmarks. (B, C, and D) Cells that contained septa between the
nucleoid and cell pole (illustrated in Fig. 1C) were analyzed for cell
length and for septum-to-pole (B), nucleoid-to-pole (C), and
septum-to-nucleoid (D) distances. A total of 434 filaments were
analyzed.
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Similar results were obtained when the measurements were made to the
center of the nucleoid instead of its edge (data not shown). This makes
it unlikely that the variability in the distance from septum to the
edge of the nucleoid was due to variations in the extent of nucleoid
shrinkage during the fixation process.
Effect of osmium tetroxide fixation.
Previous studies that led
to the nucleoid occlusion hypothesis (15) were performed
with cells that were fixed with osmium tetroxide instead of
glutaraldehyde. To exclude the possibility that the present results
were affected by glutaraldehyde fixation artifacts, the experiments
were repeated by using the osmium tetroxide fixation method.
Measurements of 180 filaments containing septa between nucleoids
and cell poles were made. The results were similar to those
described above for glutaraldehyde-fixed cells (data not shown). There
was no significant difference in the average nucleoid-to-pole distance
between the glutaraldehyde and osmium-fixed cells (P < 0.001). Septa were again clustered approximately 5 µm from the
cell pole, whereas the nucleoid-to-septum distance varied over a
wide range. These results indicate that although fixatives may
differ in their effects on nucleoid organization (22),
the effect on the parameters of the present study were negligible.
Septum placement in FtsZ DnaB
SfiA filaments.
Studies similar to those performed
with the dnaA(Ts) ftsA(Ts) double mutant
were also performed with strain WC1097(GL100) [ftsZ
null dnaB(Ts) sfiA null
(Plac-ftsZ)]. DNA replication was interrupted
by temperature upshift, which blocked elongation by inactivating the
DnaB protein. Division was prevented by repression of
Plac-ftsZ expression by growth in glucose. The
presence of the sfiA null allele prevented SOS induction of
the SfiA division inhibitor, so that division control was solely
dependent on expression of ftsZ.
The division block was not as complete as with the ftsA(Ts)
dnaA(Ts) strain described in the preceding section, as shown
by the presence of anucleate cells in the culture. This presumably reflected the residual level of FtsZ in the glucose-repressed cells. The filaments in the culture resembled those of the
ftsA(Ts) dnaA(Ts) filaments, with sizable
nucleoid-free zones between the nucleoids and the ends of the cell.
After three generations at 42°C, glucose was replaced by IPTG to
induce ftsZ expression and thereby permit division to
resume. Nucleoid-free progeny cells began to increase approximately 0.5 generation after addition of IPTG. DAPI-stained filaments that contained septa located within the polar nucleoid-free zones were analyzed for positions of septa and nucleoids, as had been done for the
ftsA(Ts) dnaA(Ts) filaments. Examples are shown
in Fig. 3. Within this population,
the average filament length was 24.5 µm (range of 4.9 to 73.3 µm), with nucleoid-to-pole distances varying between 2 and 20.9 µm.
Septa were primarily clustered at approximately 5 µm from the cell
poles, whereas the septum-to-nucleoid distance varied over a wide
range. The results (Fig. 4) were similar to those obtained with the ftsA(Ts) dnaA(Ts)
filaments (Fig. 2).
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FIG. 3.
Septation in nucleoid-free polar regions of ftsZ
dnaB(Ts) filaments. Cells of strain WC1113(GL100) were grown at
42°C for three generations in the presence of glucose, followed by 30 min in the presence of IPTG, and then fixed with glutaraldehyde and
stained with DAPI as described in Materials and Methods. The upper
panel of each pair is the fluorescence micrograph, and the lower panel
is the corresponding Nomarski image. Representative cells are shown.
Arrowheads indicate septa. Scale bar, 5 µm.
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FIG. 4.
Relationship between septum-to-pole and
septum-to-nucleoid distances in ftsZ dnaB(Ts) filaments.
Cells of strain WC1113(GL100) were grown and prepared as described
in the legend to Fig. 3, and cells that contained septa between the
nucleoid and cell pole (2,857 cells) were analyzed. See Fig. 3A for
landmarks.
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Formation of septa directly over nucleoids.
In addition to the
large number of cells in which a septum was present between the
edge of a nucleoid and the cell pole (described above), in some cells,
a septum was formed directly over a nucleoid that was located close to
a cell pole (Fig. 5). The placement of nucleoids at these positions appeared to result from residual division events that had led to formation of anucleate cells
during the period of growth under nonpermissive conditions. Cells
containing a septum directly over a polar nucleoid were more common in
shorter filaments (Fig. 6A), where the
nucleoid was more likely to extend close to the cell pole. They were
more common in the ftsZ dnaB(Ts) population (Fig. 5A), in
which the filaments were shorter due to a higher frequency of residual
division during the period of repression of ftsZ expression,
but also occurred in the ftsA(Ts) dnaA(Ts)
filaments (Fig. 5B). The positioning of septa over nucleoids resulted in a guillotine effect that fragmented the chromosome and led
to formation of partially anucleate daughter cells (Fig. 5C).
Significantly, in cells in which septation occurred directly over the
nucleoid, the positions of the septa were similar to those of the more
numerous group in which septation occurred between the edge of the
nucleoid and the cell pole (Fig. 6B). This provides additional evidence
that selection of the septation site is not directed by the position of
adjacent nucleoids.
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FIG. 5.
Septation over nucleoids. Strains WC1113(GL100)
[ftsZ null dnaB(Ts)
sfiA::Tn5
(Plac-ftsZ)] (A and C) and WC1016
[ftsA(Ts) dnaA(Ts)] (B) were grown and prepared
as described in the legends to Fig. 2 and 3. (A and B) Septa that
bisected nucleoids. (C) Cells that either lacked nucleoids or that
contained nucleoid fragments of different sizes. Scale bar, 5 µm.
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FIG. 6.
Relationship between septa and nucleoids and poles in
ftsZ dnaB(Ts) filaments. Strain WC1113(GL100) was grown
and prepared as described in the legend to Fig. 3. (A) Cells containing
septa that were located in the nucleoid-free region adjacent to a pole
(type 1) or located over a nucleoid adjacent to a pole (type 2) were
analyzed. Frequency represents the number of cells in each class/number
of cells in both classes. Cells of all cell lengths were included in
the analysis shown in the first column, whereas only cells with a
length of <20 µm were included in the analysis shown in the second
column. (B) Fifty-seven cells containing a septum located over a
nucleoid (type 2 in Fig. 6A) were analyzed as described in the legend
to Fig. 2.
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DISCUSSION |
Septal placement is independent of nucleoid position.
These
results indicate that the position of the division site is determined
by a mechanism that is independent of nucleoid position. In both
systems that were used, new septa were formed at a relatively constant
distance from the cell pole, despite the fact that a long and variable
nucleoid-free region was available. Septa were not placed at a constant
distance from the nucleoid, nor did septation occur at random positions
within the nucleoid-free region, as might be expected if the role of
the nucleoid were solely to inhibit formation of division sites in its
proximity. Instead, the positions of the new septa were related to the
position of the cell pole, leading to formation of newborn cells of
relatively uniform length.
It has recently been observed that FtsZ rings are sometimes present at
the midpoint of anucleate cells that are formed in mukB and
parC mutants that are defective in chromosome organization and partition (19). Although consistent with the idea that
division site placement is independent of nucleoid position, it cannot be determined from this result whether the FtsZ rings had been formed
before or after the division event that led to release of the
nucleoid-free daughter cell. In the former case, a relationship between
FtsZ ring placement and the position of a neighboring nucleoid would
still be possible. In the present study, this ambiguity was resolved by
examining the relative positions of nucleoid and division site within
the predivisional cell.
In a significant number of cells in the present study, septation
occurred directly over a nucleoid. This resulted in a guillotine effect, leading to formation of cells that contained incomplete nucleoids. The guillotine phenomenon has also been described in mukB (9) and smc (13)
mutants that are defective in chromosome separation after replication
has been completed. The partition defect in these cells presumably
is secondary to defects in the postreplication condensation of
daughter chromosomes (10, 13). The present study
extends these observations by showing that daughter chromosomes can be
transected by the ingrowing septum even when termination
of chromosome replication is blocked (in dnaB ftsZ cells) or when chromosome replication has been completed and
reinitiation does not occur (in dnaA ftsA cells). This
excludes the possibility that termination or initiation of replication
is required to release a local chromosome occlusion effect caused by
unreplicated or partially replicated chromosomes.
Although nucleoid position is clearly not the primary determinant of
division site placement, abnormalities in chromosome organization can
affect septal position. Thus, Sun et al. have observed that FtsZ rings
are often displaced in mukB cells and in mutants defective
in the ParC subunit of topoisomerase IV (19), and some DNA
gyrase mutations are also associated with abnormalities in cell length
distribution patterns (16). Because of the pleiotropic effects in these cases, it is not known whether the division site effects are direct or indirect results of the perturbations in chromosome organization.
It has been suggested that the formation of minicells in min
mutants is due to a defect in chromosome segregation or organization that leads to a nucleoid-free zone near the cell poles (14). An increased distance between the edges of the nucleoids and the cell
poles has been described in these mutants (2), and it was proposed that this permits minicell septa to form because of
the presence of the polar nucleoid-free zones, as predicted by
the nucleoid occlusion model. This view is contrary to the opposing
view that the polar septation events that give rise to minicells
reflect the use of residual division sites at the poles that were
derived from previous division events (6, 20). In this
regard, it may be relevant that, in the present study, there was no
evidence of minicell septa (<104 cells) despite the
presence of large nucleoid-free regions adjacent to the poles in most
cells. Thus, something in addition to nucleoid-free polar zones is
required for activation of polar minicell-producing septation events.
The septa that were formed when division was permitted to resume in the
present study were placed approximately 5 µm from the pole. This is
longer than the pole-to-septum distance in wild-type cells grown
at 30 or 42°C (unpublished observations). The reason for this
difference is unknown, although there were a number of elements
in the present experiments that could have affected the mechanism that
determines the length of newborn cells.
In a previous study, it was observed that the septum-to-nucleoid
distance was relatively constant after dnaA(Ts) cells were returned to a permissive temperature (15). In contrast, in
the present study of a dnaA(Ts) ftsA(Ts) strain,
the septum-to-nucleoid distance varied over a wide range (Fig. 4).
In both studies, the septum-to-pole positions were nonrandom,
clustering at approximately 4.5 to 5 µm from the cell pole. In
addition to the prolonged 5-h period at 42°C and the different
dnaA allele used in the prior study, a difference between
the two studies was the imposition of a division block during the
period of inhibition of DNA synthesis in the present work. As a result,
there was a much longer nucleoid-free space at the cell poles in which
the septum could have formed in the present work (nucleoid-free space,
3 to 31 µm) than in the previous study (nucleoid-free space, 3 to 8 µm). This made it relatively easy to discriminate between fixed and
random septum-to-nucleoid distribution patterns, thereby permitting a
more rigorous test of the hypothesis that septum formation occurs at a
fixed distance from the nucleoid.
Mechanism of division site identification.
If the nucleoids do
not provide the positional information that is needed to establish the
division site at its correct location, what other landmarks could be
used for this purpose? The cell poles are obvious candidates, since
division normally occurs at midcell, equidistant from the two poles.
This suggests a model in which the two cell poles act cooperatively to
determine the placement of the next division site. This could occur,
for example, if each cell pole periodically elaborated an electrical or
chemical signal that propagated along the membrane or within the
cytosol. Division site differentiation would be triggered where the
signals met at midcell [Fig. 7(a)].
Alternatively, if the signal were an inhibitor that prevented division
site formation, site differentiation would be restricted to midcell,
where the concentration of the inhibitor would fall below a threshold
level when the cells achieved a certain cell length. Since the cell
poles are derived from division sites that had been located at midcell
during preceding division cycles, the division site-identification
property of the poles would likely be inherited as part of the old
division site.
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FIG. 7.
Model for determination of division site position. The
diagram illustrates how the position of future division sites might be
directed by a signal that is periodically elaborated from the cell
poles, leading to establishment of a site at midcell (a), or from both
the cell poles and nascent division sites at midcell to establish new
sites at the cell quarters (b). In the latter case, the sites at 1/4
and 3/4 cell length are retained at the midpoint of the daughter cells
to support septum formation during the next cell cycle (3).
See text for further details.
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However, although several possible mechanisms might be used by the
poles to identify the midcell site for the next division event,
any model must accommodate the fact that the FtsZ-ZipA ring (8,
17) and the plasmolysis bays that also act as markers of future
division sites (5) can be present at 1/4 and 3/4 cell
lengths of predivisional cells prior to the onset of septation at
midcell. In this case, we suggest that the potential division site that
is present at midcell prior to septation has matured to the stage at
which it acts as a "virtual pole," working cooperatively with the
true cell poles to trigger differentiation of the potential division
sites at 1/4 and 3/4 cell lengths [Fig. 7(b)]. The subsequent division event would generate newborn cells with potential division sites already in place at midcell.
This work was supported by grants from the National Institutes of
Health (GM53276) and the Human Frontiers in Science Program (RG-386/95).
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Abstract
Introduction
