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Journal of Bacteriology, November 2000, p. 6250-6253, Vol. 182, No. 21
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Fate of the SpoIIAB*-ADP Liberated after SpoIIAB
Phosphorylates SpoIIAA of Bacillus subtilis
Chung-Sheng
Lee,
Isabelle
Lucet, and
Michael D.
Yudkin*
Microbiology Unit, Department of
Biochemistry, University of Oxford, Oxford OX1 3QU, United Kingdom
Received 15 June 2000/Accepted 10 August 2000
 |
ABSTRACT |
Phosphorylation of SpoIIAA catalyzed by SpoIIAB helps to regulate
the first sporulation-specific 
factor, F, of
Bacillus subtilis. The steady-state rate of phosphorylation is known to be exceptionally slow and to be limited by the return of
the protein kinase, SpoIIAB, to a catalytically active state. Previous
work from this laboratory has suggested that, after catalyzing the
phosphorylation, SpoIIAB is in a form (SpoIIAB*) that does not readily
release ADP. We now show that the rate of release of ADP from the
SpoIIAB*-ADP complex was much diminished by the presence of unreacted
SpoIIAA, suggesting that SpoIIAA can form a long-lived ternary complex
with SpoIIAB*-ADP in which the SpoIIAB* form is stabilized. In kinetic
studies of the phosphorylation of SpoIIAA, the ternary complex
SpoIIAA-SpoIIAB*-ADP could be distinguished from the short-lived
complex SpoIIAA-SpoIIAB-ADP, which can be readily produced in the
absence of an enzymatic reaction.
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TEXT |
Soon after the start of sporulation
in Bacillus subtilis, the cell divides asymmetrically to
give two compartments, the prespore and the mother cell, and thereafter
a pattern of differential gene expression is set up in the sporangium.
The establishment of this differential gene expression depends on
regulation of the sporulation-specific transcription factor
F (references 8, 12, and
20 and references therein). Although F is present in the predivisional cell and in the mother
cell, it is inhibited there; in the prespore, however, its activity is
released. Regulation of F depends on the three proteins
SpoIIAB, SpoIIAA, and SpoIIE. SpoIIAB is bifunctional: it can bind to
F to inhibit its activity, or it can act as a specific
protein kinase to phosphorylate SpoIIAA (1, 4, 5, 18).
SpoIIE is a specific protein phosphatase which hydrolyzes SpoIIAA-P to SpoIIAA (2, 6, 9). In the predivisional cell, most of the
SpoIIAA is present in the form of SpoIIAA-P (17), which does
not interact with SpoIIAB (16); as a result, SpoIIAB is free
to inhibit F. But at or a little before the time of
asymmetric division, SpoIIE is activated and SpoIIAA-P is hydrolyzed to
give SpoIIAA. The interaction of this free SpoIIAA with SpoIIAB
prevents the latter from inhibiting F in the prespore
(4, 7, 10, 11, 17).
This system has a number of distinctive features that help to
explain its biological function. First, in the prespore the SpoIIAB
kinase and SpoIIE phosphatase are active simultaneously, and
SpoIIAA is continually cycled between the nonphosphorylated and the
phosphorylated forms (17). Second, the activity of SpoIIE is
much higher than that of SpoIIAB (15), and hence in the
prespore all (or almost all) of the SpoIIAA is in the nonphosphorylated form (9, 11, 13). Third, the intracellular concentrations of
SpoIIAB and F are equal, so that there is only just
enough SpoIIAB to inhibit F; thus, the sequestration of
even a fraction of the SpoIIAB in an alternative reaction will liberate
some F activity (17). Finally, the
phosphorylation catalyzed by SpoIIAB is extremely slow, with the result
that at any given time much of the SpoIIAB is in fact sequestered in
this reaction (17, 19).
The kinetics of the phosphorylation of SpoIIAA by SpoIIAB in vitro
follow a biphasic time course, with a moderate rate giving way to a
very slow steady-state rate (about 0.6 × 10
3 mol of
SpoIIAA phosphorylated per mol of SpoIIAB per s) after 1 mol of SpoIIAA
has been phosphorylated per mol of SpoIIAB (17). This
feature suggests that the rate-determining step in the enzymatic reaction is that in which the enzyme returns to a catalytically active
form after each round of phosphorylation (17). In a detailed study of the reaction mechanism, Najafi et al. (19)
suggested the minimal scheme shown in Fig.
1. A particular feature of this scheme
was the proposal that, after liberating the product SpoIIAA-P, SpoIIAB
is in a special conformation, SpoIIAB*, which releases ADP
exceptionally slowly. It was the slow relaxation of this form to
SpoIIAB that was presumed to allow the release of ADP and to determine the overall rate of the enzymatic reaction.
Duncan et al. (7) and Garsin et al. (10) have
given an alternative account of the phosphorylation of SpoIIAA that
does not include a proposal for an unusual conformation of SpoIIAB. These workers suggest that SpoIIAA-P is produced by a reaction of
SpoIIAA with a SpoIIAB-F-ATP complex. This reaction
liberates SpoIIAB-ADP, which interacts with another molecule of SpoIIAA
to form a long-lived SpoIIAA-SpoIIAB-ADP complex. The dissociation of
this complex is then necessary to allow phosphorylation of SpoIIAA to proceed.
In the present communication, we produce further evidence for the
existence of SpoIIAB*, give a fuller account of the return of
SpoIIAB*-ADP (via a ternary complex with SpoIIAA) to the
catalytically active form, and assess the significance of the unusual
properties of the system for the regulation of F in the cell.
SpoIIAB*-ADP forms a complex with SpoIIAA.
The experiments
that led to the discovery of SpoIIAB* involved the phosphorylation of
excess SpoIIAA in the presence of limiting concentrations of SpoIIAB.
It seemed possible that, in such conditions, SpoIIAB*-ADP liberated
after phosphorylating SpoIIAA could bind to another molecule of SpoIIAA
to give a ternary complex and that it is the slow dissociation of this
complex that determines the steady-state rate of the phosphorylation
reaction. (This suggestion would be parallel to that made by
Duncan et al. [7] and Garsin et al.
[10], who, however, do not include SpoIIAB* in their scheme.) We therefore designed experiments to see whether the presence of excess SpoIIAA reduces the rate of release of ADP from its
complex with SpoIIAB*. SpoIIAA proteins were purified as described
previously (16). SpoIIAA and [
-32P]ATP (1 µM each) were incubated with 1 µM SpoIIAB in buffer A (19) at 30°C for 20 min. When samples of this mixture were
separated by nondenaturing polyacrylamide gel electrophoresis, about
60% of the SpoIIAA was found to have been converted to SpoIIAA-P. By
centrifuging a sample through a Centricon 10 filter and counting the
radioactivity in the filtrate, we found that some 10% of the total
radioactivity remained bound to protein. Of the 90% of the radioactivity that was free in solution, thin-layer chromatography (3) showed that about 40% was ATP and about 60% was ADP.
It appears that under these conditions the phosphorylation of SpoIIAA by ATP fails to proceed to completion. (We note that the
Km of the phosphorylation reaction for ATP is
1.4 µM and the Ki for ADP is 1.0 µM
[19].)
The mixture just described, which included protein-bound
[
-
32P]ADP, was then divided into two equal portions,
and one of these
was supplemented with additional SpoIIAA (10 µM).
After 1 min,
we added 10 µM ATP-
-S [adenosine
5'-O-(3-thiotriphosphate)],
a nonhydrolyzable analog of ATP, to both
mixtures. At intervals,
the mixtures were centrifuged through a
Centricon 10 filter, and
the radioactivity in samples of the filtrates
was counted. The
two curves in Fig.
2a
show the results. In the portion to which
excess SpoIIAA has not been
added (upper curve), [
-
32P]ADP (see below) was
released rapidly after the addition of ATP-
-S.
By the time the first
sample could be processed, only a small
percentage of the radioactivity
remained bound to protein, and
this final quantity was released within
5 to 6 min (upper curve
in Fig.
2a). But in the portion to which excess
SpoIIAA had been
added before the ATP-
-S, the
[
-
32P]ADP was released only very slowly from the
protein-bound form
(lower curve in Fig.
2a); even after 60 min, some
ADP was still
bound to the protein complex.
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FIG. 2.
(a) Effect of SpoIIAA on release of ADP from
SpoIIAB*-ADP. [-32P]ATP was used to phosphorylate
SpoIIAA in the presence of SpoIIAB. After the addition of ATP--S,
samples were subjected to filtration through a Centricon filter. The
radioactivity of the filtrate was measured and is expressed as a
percentage of the radioactivity in the incubation mixture. The release
of ADP was measured in the absence ( ) and in the presence ( ) of
additional SpoIIAA. (b) Radioactivity released after incubation
of SpoIIAA and SpoIIAB with [-32P]ATP. (c) Effect of
SpoIIAAL90A on release of ADP from SpoIIAB*-ADP. The experiment
shown in panel a was repeated, and the release of ADP was measured in
the absence () and in the presence () of added SpoIIAAL90A.
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We interpret these findings in the following way. In the first mixture,
the addition of ATP-
-S allows the release of
[
-
32P]ADP from SpoIIAB to be observed; this release is
complete within
some 6 min. In the second mixture (to which excess
SpoIIAA is
added), SpoIIAA forms a complex with
SpoIIAB*-[
-
32P]ADP. This ternary complex decays very
slowly, and the rate of
its decay can be followed by monitoring the
release of [
-
32P]ADP. By comparing the two curves, we
see that the presence of
SpoIIAA diminished the rate of release of ADP
by a factor of more
than 10-fold, suggesting that the
SpoIIAA-SpoIIAB*-ADP complex
is remarkably long-lived.
To test this interpretation, we did two further kinds of experiment.
First, we proved that it was ADP and not ATP that was
released from the
ternary complex by repeating the experiment
reported in the lower curve
of Fig.
2a, but substituting [
-
32P]ATP for
[
-
32P]ATP. The results (Fig.
2b) showed that no
radioactivity was
released in these circumstances. Second, we repeated
the experiment
again, but instead of adding excess wild-type SpoIIAA
after the
20 min of initial incubation, we added SpoIIAAL90A, a mutant
form
of SpoIIAA that can be readily phosphorylated but does not make
a
stable complex with SpoIIAB in the presence of ADP (C.-S. Lee
and
M. D. Yudkin, unpublished results). The results (Fig.
2c)
show
that the release of ADP from its complex with SpoIIAB was
scarcely
affected by the presence of SpoIIAAL90A. The striking
contrast between
the effect of the wild-type protein and that
of the mutant protein
strongly suggests that the slow release
of [
-
32P]ADP
shown in the lower curve of Fig.
2a reflects the gradual
decay of a
SpoIIAA-SpoIIAB*-ADP complex. The rate of loss of radioactivity
from
the complex that included wild-type SpoIIAA corresponded
to about
0.4 × 10
3 mol of ADP released per mol of SpoIIAB
per s, which is very similar
to the steady-state rate of the overall
phosphorylation reaction.
It seems likely, then, that it is the
dissociation of the SpoIIAA-SpoIIAB*-ADP
complex that determines the
rate of phosphorylation and accounts
for its exceptional sluggishness.
The mechanism of dissociation
of the complex is considered in more
detail
below.
Given the results shown in Fig.
2, one might predict that in a
mixture containing SpoIIAA, SpoIIAB, and ATP, the SpoIIAB would
remain in a SpoIIAA-SpoIIAB*-ADP complex until all the SpoIIAA
had been
phosphorylated and thereafter would be set free. We tested
this
prediction by incubating 20 µM SpoIIAA and 1 µM SpoIIAB with
1 mM
ATP at 30°C, taking samples at intervals, and subjecting
them to
nondenaturing gel electrophoresis, in which SpoIIAA-SpoIIAB-ADP
complexes can be separated from SpoIIAB (
4). The results
(Fig.
3) show that SpoIIAB remained
trapped in the complex until all
the SpoIIAA had been converted to
SpoIIAA-P, when it was released.
It follows from this finding that in a
situation in which there
is an infinite supply of SpoIIAA (which is
presumed to be the
case in the prespore when SpoIIAB and SpoIIE are
both active),
SpoIIAB will never be released from the
SpoIIAA-SpoIIAB*-ADP complex
and will therefore remain unavailable to
inhibit
F.
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FIG. 3.
Trapping of SpoIIAB in a complex with SpoIIAA and ADP
and its release after phosphorylation is completed. Samples were taken
at the times shown and subjected to nondenaturing gel electrophoresis.
The positions of SpoIIAA, SpoIIAA-P, SpoIIAB, and SpoIIAA-SpoIIAB*-ADP
are indicated by arrows.
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|
Confirmation of the existence of SpoIIAB*.
In the light of the
above results, it might be suggested that one could interpret the
biphasic kinetics of the phosphorylation of SpoIIAA in the following
way. After 1 mol of SpoIIAA has been phosphorylated per mol of SpoIIAB,
one equivalent of ADP is present in the mixture. The ADP and SpoIIAB
could then interact with unreacted SpoIIAA to form SpoIIAA-SpoIIAB-ADP.
This is a deadend complex, whose dissociation is essential for
phosphorylation to proceed, and the subsequent diminished rate of the
reaction (about 0.4 × 103 s1
see
above) could be explained if dissociation of the complex were very
slow. Although this suggestion seems incompatible with the measured
rate of dissociation of SpoIIAA-SpoIIAB-ADP, which is about 15 × 103 s1 (17), we designed an
experiment to see if we could distinguish between SpoIIAA-SpoIIAB*-ADP
and SpoIIAA-SpoIIAB-ADP. If the two are identical and SpoIIAB* does not
exist (that is, if the SpoIIAB that is released after phosphorylating
SpoIIAA is no different from the normal SpoIIAB molecule), it should be
possible to inhibit the phosphorylation reaction from the outset by
adding 1 mol of ADP per mol of SpoIIAB. We therefore followed the
phosphorylation of 50 µM SpoIIAA by 250 µM
[-32P]ATP in the presence of 0.5 µM SpoIIAB, with
and without 5 µM ADP (a 10-fold molar excess over SpoIIAB). Protein
was precipitated with trichloroacetic acid, and its radioactivity was
determined (17). As Fig. 4
shows, the addition of ADP had no effect on the initial rate of
reaction. (A repetition of this experiment, but with SpoIIAB
preincubated with ADP before the addition of SpoIIAA and
[-32P]ATP, yielded similar results [not shown].)
After about 3 min the rate of phosphorylation slowed to one-third of
its original value, both in the reaction to which no ADP had been added
and in that which had been supplemented with ADP (Fig. 4). At this point, measurement of the radioactivity that had been incorporated into
SpoIIAA-P suggested that the ADP that had been generated by the
phosphorylation reaction amounted to between 1.0 and 1.1 mol per mol of
SpoIIAB.
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FIG. 4.
Time course of phosphorylation of SpoIIAA. SpoIIAA (50 µM) was incubated with 250 µM [-32P]ATP and 0.5 µM SpoIIAB in the absence () or presence () of 5 µM ADP. The
graph shows the radioactivity in trichloroacetic acid-insoluble protein
(17). The dashed line is an extension of the gradient of
incorporation over the first few minutes, to emphasize the difference
between the pre-steady-state and the steady-state rates of
incorporation.
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In the light of the results presented in Fig.
2, we attribute the
change in rate after 3 min to the formation of a long-lived
SpoIIAA-SpoIIAB*-ADP complex, whose dissociation is now the
rate-determining
step in the phosphorylation of further SpoIIAA
molecules. The
formation of this complex evidently depends on the
ability of
SpoIIAB to bind to ADP even in the presence of a 500-fold
excess
of ATP, quite unlike the normal situation, in which SpoIIAB has
about the same affinity for ADP and ATP (
14). In other
words,
the SpoIIAB that has just phosphorylated SpoIIAA and thus
generated
ADP readily makes a complex with a molecule of
(unphosphorylated)
SpoIIAA, whereas the SpoIIAB present at the
beginning of the reaction
fails to make such a complex with SpoIIAA
even when a 10-fold
higher concentration of ADP is added to the
mixture. We conclude
that SpoIIAB that has taken part in the reaction
in which SpoIIAA
is phosphorylated is in an unusual conformation (the
conformation
that we have called SpoIIAB* [
19]), in
which it is tightly complexed
with ADP and interacts readily with
SpoIIAA.
A scheme that takes account of all these results is presented in
Fig.
5. Given the characteristic biphasic
time course of
the phosphorylation reaction, it is clear that the
rate-determining
step in this scheme must be later than the step in
which SpoIIAA-P
is released
that is, it must be either the relaxation
of SpoIIAB*
to SpoIIAB or the dissociation of the
SpoIIAA-SpoIIAB-ADP complex.
However, the rate constant for the latter
step is known to be
some 20 times greater than the overall rate
constant for the phosphorylation
(
17; see above). We
therefore conclude, as before (
19), that
the rate of the
reaction is limited by the conformational change
from SpoIIAB* to
SpoIIAB. The results presented in Fig.
2 suggest
that the presence of
SpoIIAA in the ternary complex stabilizes
the SpoIIAB* conformation of
SpoIIAB.
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FIG. 5.
Scheme of the mechanism of phosphorylation of SpoIIAA
(A) by SpoIIAB (B), taking into account the results described in this
communication.
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|
Significance of the results for the regulation of F
in the cell.
After asymmetric septation, SpoIIAB and SpoIIE are
both active in the prespore, and SpoIIAA therefore cycles continually
between the phosphorylated and the nonphosphorylated form
(17). However, the activity of SpoIIE is much greater than
that of SpoIIAB (15), and as a result SpoIIAB is constantly
supplied with SpoIIAAwhich is not only its substrate, but also its
partner in the noncovalent complex. Every time a molecule of SpoIIAB
catalyzes the phosphorylation of SpoIIAA, it is released as
SpoIIAB*-ADP, and it can then interact with another molecule of
SpoIIAA. The resulting noncovalent complex, SpoIIAA-SpoIIAB*-ADP, is
enzymatically inactive, and the rate of its decay determines the rate
at which SpoIIAB becomes available either to phosphorylate SpoIIAA or
to inhibit F. Since the SpoIIAA-SpoIIAB*-ADP complex is
long-lived by virtue of the slow relaxation of AB* to AB, and since the
intracellular concentrations of SpoIIAB and F are equal
(17), the effect of these interactions is to leave many
F molecules uninhibited by SpoIIAB. Thus, activation of
F depends on the sequestration of SpoIIAB in long-lived
complexes that result from the phosphorylation reaction and which one
might call postphosphorylation complexes.
Several years ago it was generally accepted that there were two ways in
which SpoIIAA and SpoIIAB could interact
in the presence
of ATP
SpoIIAB catalyzed the phosphorylation of SpoIIAA, and in
the presence
of ADP the two proteins formed a noncovalent complex.
These two
interactions were regarded as alternatives, and the
choice between them
was believed to depend on the local concentration
of ATP and/or ADP
(
1,
4,
7,
16). The results presented
here show that the two
interactions are not alternatives but rather
(as hypothesized by Garsin
et al. [
10]) occur successively.
Together, the two
interactions constitute a subtle mechanism for
releasing
F from inhibition in the prespore. Once asymmetric
septation has
been completed, this activation of
F
enables differential gene expression to get under way in the
two
compartments of the
sporangium.
| |
ACKNOWLEDGMENTS |
We are grateful to D. A. Harris for much valuable advice and
for his helpful comments on the manuscript.
This work was supported by grants from the Biotechnology and Biological
Sciences Research Council.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Biochemistry, University of Oxford, South Parks Road, Oxford OX1 3QU, United Kingdom. Phone: 44 1865 275302. Fax: 44 1865 275297. E-mail: mdy{at}bioch.ox.ac.uk.
| |
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Journal of Bacteriology, November 2000, p. 6250-6253, Vol. 182, No. 21
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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