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Previous Article | Next Article 
Journal of Bacteriology, September 1999, p. 5476-5481, Vol. 181, No. 17
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Regulation of Synthesis of the Bacillus
subtilis Transition-Phase, Spore-Associated Antibacterial
Protein TasA
Axel G.
Stöver and
Adam
Driks*
Department of Microbiology and Immunology,
Loyola University Medical Center, Maywood, Illinois 60153
Received 31 March 1999/Accepted 22 June 1999
 |
ABSTRACT |
Previously, we identified a novel component of Bacillus
subtilis spores, called TasA, which possesses antibacterial
activity. TasA is made early in spore formation, as cells enter
stationary phase, and is secreted into the medium as well as deposited
into the spore. Here, we show that tasA expression can
occur as cells enter stationary phase even under sporulation-repressing
conditions, indicating that TasA is a transition-phase protein.
tasA and two upstream genes, yqxM and
sipW, likely form an operon, transcription of which is
under positive control by the transition-phase regulatory genes
spo0A and spo0H and negative control by the
transition phase regulatory gene abrB. These results are
consistent with the suggestion that yqxM, sipW,
and tasA constitute a transition phase operon that could
play a protective role in a variety of cellular responses to stress
during late-exponential-phase and early-stationary-phase growth in
B. subtilis.
| |
INTRODUCTION |
When confronted with nutrient
deprivation, B. subtilis can choose from a large set of
alternative responses such as the production of antibiotics and
proteases, the uptake of exogenous DNA (the state of competence), and
the formation of a dormant cell type called the spore (20).
Previously, we identified a novel spore-associated protein, called
TasA, which possesses an antibacterial activity and is also secreted
into the culture supernatant at the beginning of sporulation
(19). tasA is immediately downstream of
sipW (Fig. 1A) (9),
encoding a signal peptidase (22, 23) that is required for
the maturation and secretion of TasA (19). sipW is downstream of and partially overlaps yqxM, whose function
is unknown. The proximity of these three genes and the functional relationship between SipW and TasA raise the possibility of coordinate regulation of this gene cluster.
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FIG. 1.
The yqxM sipW tasA locus and DNA constructs.
(A) The yqxM sipW tasA locus. Open boxes represent genes,
and the region likely to contain the promoter(s) is indicated by a
bracket. Restriction sites are indicated. (B) Transcriptional reporter
fusion constructs. Black boxes represent the lacZ gene of
E. coli. Names of strains bearing these fusions are
indicated. Fusions were inserted by marker replacement at the
amyE locus except for sipW-lacZ (a gift from
J. M. van Dijl), which was integrated by single-reciprocal
integration, indicated by the dotted line (to generate AGS307).
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Previously, we found that the production of TasA requires Spo0A and
H, molecules that guide regulation at the juncture
between exponential and stationary phases (5) (Fig.
2A), consistent with TasA synthesis early
in sporulation (19). To examine the possibility that TasA is
a transition-phase protein and to deepen our understanding of the
regulatory controls on the expression of tasA and the
adjacent genes, we have studied the regulation of TasA synthesis during a variety of growth conditions, defined 5' sequences required for
tasA expression, and identified some of the relevant
regulatory factors.
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FIG. 2.
Regulation of transition-phase gene expression and a
model for the possible regulation of the yqxM sipW tasA
operon. (A) Summary of the roles of Spo0A, H, and AbrB
on transition-phase gene expression. The long arrow on the left
indicates the influence of factors controlling the cellular
concentration of Spo0A~P, which in turn determines whether the cell
will express sporulation (Spo) genes, competence (com) genes, or genes
associated with another transition phase choice (on the right). Not all
transition-phase genes are controlled directly by Spo0A. (B) A
speculative model for transcriptional control of the operon. Spo0A and
H direct expression. Separately, an as yet unidentified
additional sigma factor also directs expression. AbrB can repress both
events. Although a single promoter is illustrated, multiple promoters
may be present.
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MATERIALS AND METHODS |
Strains, media, and recombinant DNA procedures.
Strains,
plasmids, and primers for PCR are listed in Tables
1 and 2.
All recombinant DNA procedures were performed by using standard
procedures (16), and manipulations in B. subtilis
were carried out according to procedures in reference
2. Cells were grown in Difco sporulation medium
(DSM) (2) unless otherwise indicated. 2×YT, Luria-Bertani
(LB), and Terrific broth (TB) media (16) and King's B
medium (8) were prepared as described elsewhere.
Transcriptional fusions to lacZ.
First, we digested
the amyE replacement vector pDG268 (6) with
EcoRI and HindIII, purified the larger
resulting fragment, and ligated it to the
EcoRI-HindIII fragment of pSL1180 containing the multiple cloning site, creating pAGS38. Next, we amplified the
yqxM sipW tasA locus by PCR using primers OL109 and OL110 and digested the fragment with NheI and NotI. We
then cloned the fragment between the NheI and
NotI sites of pAGS38, creating the tasA-lacZ
transcriptional fusion plasmid pAGS42. To make the yqxM-lacZ transcriptional fusion (in pAGS43), we digested pAGS42 with
NheI and HindIII and ligated the smaller
resulting DNA fragment into similarly digested pAGS38. pAGS42 and
pAGS43 were linearized with KpnI and used to transform a
variety of strains to chloramphenicol resistance (Table 1). We made
pAGS51, pAGS53, pAGS54, pAGS55, pAGS56, pAGS57, and pAGS58 by
essentially the same procedure but used oligonucleotides OL116 and
OL110, OL131 and OL110, OL132 and OL110, OL133 and OL110, OL134 and
OL110, OL135 and OL110, and OL136 and OL110, resulting in strains
AGS340, AGS376, AGS377, AGS378, AGS379, AGS380, and AGS381,
respectively. Strain 8G5::pLGW201, bearing
sipW-lacZ as a single reciprocal (Campbell-type) integration at sipW (22), was a kind gift from J. M. van
Dijl. We moved this fusion into PY79 by transformation, resulting in
strain AGS307.
Determination of relative TasA levels and 
-galactosidase
assays.
Cells were harvested 5 h after the end of exponential
phase, pelleted, and then lysed by resuspension in 25 mM Tris-HCl (pH 7.5)-50 mM glucose-10 mM EDTA-100 µg of lysozyme per ml followed by a 10-s burst of sonication (using a Fisher Dismembrator). We determined the concentration of total protein in each sample with a
bicinchoninic acid protein assay reagent kit (Pierce) and then carried
out electrophoresis on 12% polyacrylamide gels and Western blot
analysis (19). We used a Hewlett-Packard ScanJet 6200C and
AlphaImager 2000 version 4.03 software (Alpha Innotech Corporation) to
determine the amounts of TasA relative to total protein in each strain
and divided these ratios by the ratio of TasA to total protein in
wild-type cells. We carried out -galactosidase assays as described
elsewhere (2) except that the reaction was performed at
37°C instead of 30°C.
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RESULTS AND DISCUSSION |
Medium requirements for TasA synthesis.
We previously found
that TasA synthesis began as cells entered stationary phase during
growth in sporulation medium (DSM). To determine whether TasA could be
made independently of the decision to sporulate, we used Western blot
analysis to follow the steady-state accumulation of TasA in 2×YT
medium (in which sporulation was decreased to 0.01% [data not
shown]). We first detected TasA at the beginning of stationary phase
and found that it was present for at least 7 h (Fig.
3 and data not shown). We also detected TasA in cells grown in King's B, LB, or TB medium, in which
sporulation occurred in less than 0.01% of the cells (data not shown).
Therefore, TasA is a transition-phase protein that first appears at the
beginning of stationary phase.
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FIG. 3.
Western blot analysis of TasA during growth in 2×YT.
Extracts of cells grown in 2×YT were prepared at the indicated times
before and after the onset of stationary phase (T0). After
fractionation by sodium dodecyl sulfate-polyacrylamide gel
electrophoresis and electrotransfer to polyvinylidene difluoride
membranes, TasA was detected with an anti-TasA antibody. Molecular mass
is indicated in kilodaltons on the left.
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Sequences required for tasA expression.
The
arrangement of yqxM, sipW, and tasA
suggested they form an operon (Fig. 1A). As an initial test of this
possibility, we compared the level of tasA-lacZ expression
in a strain missing all of the sequences upstream of the
yqxM open reading frame (AGS340) with the level in a strain
in which 351 bp upstream of yqxM were retained (AGS303). In
strain AGS303, tasA-lacZ expression began at about 15 min
before the beginning of stationary phase and maintained a significant
level for at least 7 h (Fig. 4A),
similarly to the timing of appearance of TasA (Fig. 3 and reference
19). Consistent with this, we were able to readily
detect TasA by Western blot analysis when only 351 bp of upstream
sequence were present (data not shown). The removal of the upstream
sequence reduced tasA expression almost to background levels
(Fig. 4A). Likewise, we did not detect TasA by Western blot analysis
when the upstream sequence was removed (data not shown).
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FIG. 4.
-galactosidase activity in cells bearing
yqxM-, sipW-, or tasA-lacZ. All
strains harbor either sipW-lacZ (AGS301),
yqxM-lacZ (AGS307), no fusion (PY79 and JH642), or
tasA-lacZ (all remaining strains). In each plot, the onset
of stationary phase (time zero) is indicated by an arrow. (A) Fusions
to tasA, sipW, or yqxM and a
tasA-lacZ fusion in which the 351 bp upstream of
yqxM have been deleted. Strains tested: AGS301
(yqxM-lacZ) ( ), AGS307 (sipW-lacZ) ( ),
AGS303 (tasA-lacZ) ( ), AGS340 (yqxM upstream
sequences deleted, tasA-lacZ) ( ), and PY79 ( ). (B)
tasA-lacZ fusions retaining various regions upstream of
yqxM. Strains tested: AGS303 (retaining 351 bp) (),
AGS376 (281 bp) (), AGS377 (264 bp) (), AGS378 (233 bp) (),
AGS379 (114 bp) ( ), AGS380 (40 bp) (+), AGS381 (30 bp) ( ), and
PY79 (). (C) Effects of spo0A and spo0H.
Strains tested: AGS303 (wild type) (), AGS305
(spo0H HindIII-EcoRI::cat::Specr)
(), AGS313 (spo0A::Ermr) (),
and PY79 (). (D) Effects of abrB. Strains tested: AGS303
(wild type) (), AGS351
(abrB::Tn917) (), AGS352
(abrB::cat
spo0HHindIII-EcoRI::cat::Specr)
(), AGS392
(abrB::Tn917::pSpc101
spo0A::Ermr) (), and PY79 ().
(E) Effect of deletion of the H-driven promoter of
spo0A. Strains tested: AGS387 (wild type) (), AGS367
(spo0APs) (), and JH642 (). (F) Effects of alleles
of spo0A deficient in A-dependent gene
expression. Strains tested: AGS303 (wild type) (), AGS361
(spo0A::pSPC101) (), AGS362
(spo0A::pSPC101-S233P) (×), AGS363
(spo0A::pSPC101-G227R) (), AGS364
(spo0A::pSPC101-F236S) (), AGS365
(spo0A::pSPC101-V240A) (+), AGS366
(spo0A::pSPC101-V240G K265R) (), and PY79
(). Units of -galactosidase activity are defined in Materials and
Methods. Scales along the y axis vary from panel to panel;
in particular, the scale in panel D is compressed.
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To study the timing of expression of the genes in this locus, we
measured -galactosidase activities of strains harboring transcriptional fusions of yqxM, sipW, and
tasA to lacZ of E. coli (strains
AGS301, AGS307, and AGS303, respectively [Fig. 1B]). We found that
expression of all three genes initiated at the beginning of
stationary-phase growth (Fig. 4A), consistent with the timing of TasA
production (Fig. 3 and reference 19). The wild-type strain, without the tasA-lacZ fusion (PY79), showed
background levels of -galactosidase activity (and a white color on
solid indicator medium [data not shown]). For unknown reasons, the
levels of expression of the yqxM-lacZ and
sipW-lacZ fusions were consistently lower than that of
tasA-lacZ. To further define the upstream region needed for
tasA-lacZ transcription, we generated a set of fusions missing progressively more of the 351-bp region (Fig. 1B). We found
significant levels of tasA-lacZ expression when 233 bp or more upstream of yqxM were retained but detected no
expression when 114 or fewer bp of upstream sequence were present (Fig.
4B). These results suggest that yqxM, sipW, and
tasA constitute an operon and that the sequences required
for tasA expression under these conditions of growth are
confined to a region 233 bp upstream of yqxM. They also
argue against the presence of strong promoters between the beginning of
the yqxM open reading frame and the tasA open
reading frame.
Roles of Spo0A, H, and AbrB in tasA
transcription.
We found background levels of -galactosidase
activity in strains bearing mutations in spo0A (AGS313) and
spo0H (AGS305) (Fig. 4C), suggesting that Spo0A and
H are required for tasA expression. We
detected about 10-fold-higher levels of tasA-lacZ expression
in a strain bearing an abrB mutation (AGS351) (Fig. 4D),
indicating that AbrB represses tasA expression. We also
found that TasA steady-state levels in two strains bearing null
mutations in abrB (AGS347 and AGS348) were approximately sixfold higher than in the wild type (Table
3).
The effect of AbrB on tasA expression could be indirect, via
repression of spo0H (25) (Fig. 2A). If this is
true, then tasA-lacZ expression should be at background
levels in an abrB spo0H double mutant. In such a strain
(AGS352), expression of tasA-lacZ occurred about 2 h
earlier than in the wild type and ultimately was three- to fivefold
higher than in the wild type, similarly to an abrB strain
(AGS351) (Fig. 4D). TasA levels in strains bearing abrB and
spo0H mutations (AGS349 and AGS350) were somewhat higher
than in the wild type (Table 3). From these data, we infer that AbrB does not repress tasA expression solely by inhibition of
spo0H expression. These results also suggest that AbrB
represses a H-independent mechanism of tasA
expression that acts prior to the onset of stationary phase. In
contrast to the abrB mutant, in the double mutant
tasA expression did not remain high but rather decreased
over time. The difference in tasA expression between the two
strains further argues that AbrB also represses a post-exponential H-dependent phase of expression. Apparently, when
abrB is intact, this phase of H-directed
expression is not completely repressed, accounting for the wild-type
pattern of tasA expression.
One interpretation of these findings is the presence of two promoters
upstream of yqxM, one of which is H and Spo0A
dependent and other of which utilizes a second sigma factor and is
Spo0A independent. To determine whether a H-independent
promoter might reside within the already identified 351-bp region
upstream of the yqxM open reading frame, we measured -galactosidase activities in spo0H abrB tasA-lacZ strains
missing various portions of this region. We detected
tasA-lacZ expression when 233 bp or more were present but
not when only 114 bp or fewer remained (data not shown). Therefore, if
a second promoter exists, its activity requires sequences within the
same 233-bp region required by the H-dependent promoter.
Spo0A could affect tasA expression indirectly, via
repression of abrB (Fig. 2A). If this is so, then
tasA expression in the abrB spo0A strain would
appear similar to what was seen in the strain bearing only the
abrB mutation. If, on the other hand, Spo0A directly
activated tasA expression, then tasA expression in the abrB spo0A strain would resemble expression in the
abrB spo0H strain. We addressed this issue by measuring
tasA-lacZ expression in an abrB spo0A strain
(AGS392). We found that the pattern of expression resembled that of the
abrB spo0H strain (AGS352) (Fig. 4D). These data indicate
that Spo0A does not act exclusively through AbrB to activate
tasA expression and are consistent with the possibility that
Spo0A binds the tasA promoter. A possible Spo0A-binding site is present between nucleotides 
32 and 38 relative to the beginning of the yqxM open reading frame.
The finding that tasA expression depends on H
raised the possibility that tasA expression requires
H-directed expression of spo0A (1,
15). To test this, we measured tasA-lacZ expression
and TasA steady-state levels in a strain in which spo0A is
missing its H-dependent promoter
(spo0APs), placing spo0A expression under the
control solely of A (18). We compared
-galactosidase activity in a spo0APs
tasA-lacZ-bearing strain (AGS367) to the activity in
congenic strains harboring either the tasA-lacZ fusion
(AGS387) or no fusion (JH642). We found that the levels of
tasA-lacZ expression (Fig. 4E) and TasA synthesis (Table 3)
were significantly above background, suggesting that the absolute
requirement for H is not due to its action at the
spo0A promoter. Because the spo0APs strain
(AG1242) cannot sporulate (18), this result also supports our view that TasA is not exclusively a sporulation protein.
Role of A in tasA transcription.
It
is possible that tasA expression requires Spo0A-dependent
A-directed gene expression. To test this, we made use of
strains carrying special alleles of spo0A
(spo0A::pSPC101-G227R,
spo0A::pSPC101-S233P, spo0A::pSPC101-F236S,
spo0A::pSPC101-V240A, or
spo0A::pSPC101-V240G K265R [4]),
encoding versions of Spo0A that are unable to activate the
A-dependent genes spoIIE and
spoIIG but are able to direct expression of at least one
H-dependent gene (spoIIA) to different
degrees. We compared tasA-lacZ expression and TasA
steady-state levels in the wild-type strain (AGS303) and the
spo0A null mutant strain (AGS361) with strains bearing these
altered spo0A alleles (AGS362, AGS363, AGS364, AGS365, and
AGS366). The levels of tasA-lacZ expression (Fig. 4F) and of
TasA (Table 3) varied in strains bearing the altered spo0A alleles but were significantly above background in all cases. These
data are consistent with the possibility that tasA
expression largely relies on Spo0A acting together with
H.
To determine whether the specialized sigma factors B or
D (3) are needed for TasA synthesis, we used
Western blot analysis to determine if TasA was present in extracts of a
sigB::cat strain (AGS368) or a
sigD::Kanr strain (AGS306). In both
strains, TasA levels were similar to those in wild type (data not
shown), indicating that neither B nor D
is absolutely required for TasA production.
Our results suggest that Spo0A and H, directly or
indirectly, activate expression of the operon (Fig. 2B). The
involvement of H in tasA expression is
supported by the results of Serrano et al. (17), who showed
that tasA was expressed during vegetative growth when
spo0H expression was activated prematurely, using an
inducible promoter. The expression of tasA in a strain
missing the H-directed spo0A promoter
(spo0APs) argues against the possibility that the major
role of H in tasA expression is at the level
of spo0A expression and further implies that high levels of
Spo0A are not required for tasA expression (18).
AbrB is likely to repress both H-dependent and
H-independent phases of tasA expression,
possibly originating from two promoters. Therefore, AbrB appears to
serve at least two roles in tasA expression. First, AbrB
prevents inappropriate tasA expression during exponential
phase, as it does for many other genes (20). Second, it
reduces tasA expression during post-exponential-phase growth.
We have not yet identified the start site(s) of transcription of the
operon. As yet, primer extension and 5'RACE (rapid amplification of 5'
cDNA ends) methods have yielded ambiguous results. This could be due to
a low level of message and/or secondary structure at the 5' end of the message.
We do not know the significance of the coordinate regulation of
yqxM, sipW, and tasA. However, the
clustering and coregulation of a specialized signal peptidase gene with
one or more substrate-encoding genes may occur more widely than is
usually appreciated. Interesting examples of this occur in
Bacillus subtilis (natto), which is well known to harbor a
variety of cryptic plasmids (21, 24). Two such plasmids,
pTA1015 and pTA1040, encode proteins very similar to the chromosomally
encoded B. subtilis signal peptidase SipS (11,
12). Intriguingly, in each of these plasmids, an open reading
frame of unknown function, encoding a plausible signal peptide, sits
immediately upstream of the signal peptidase gene. Apparently, these
pairs of genes form operons. The potentially secreted gene products
could be substrates for the encoded signal peptidases. The additional
presence of genes encoding response regulator aspartate phosphatases
(13, 14) in some of these plasmids suggests a role in
post-exponential-phase responses. Possibly, the coordinate expression
of a signal peptidase gene with one or more genes encoding substrates
provides an important level of control over secretion during
early-stationary-phase growth.
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ACKNOWLEDGMENTS |
We thank Jean Greenberg, John Helmann, Shawn Little, Mark
Strauch, and Phil Youngman for critically reading the manuscript and
for helpful discussions. We thank Janet Hatt, John Helmann, Alan
Grossman, Phil Youngman, and Jan Maarten van Dijl for gifts of strains.
We especially acknowledge the advice of John Lopes and the editor. We
also acknowledge the excellent technical assistance of Dong Chae.
This work was supported by Public Health Service grant GM539898 from
the National Institutes of Health and the Schweppe Foundation. A.G.S.
was funded, in part, by a Schmitt dissertation fellowship.
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FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Microbiology and Immunology, Loyola University Medical Center, 2160 South First Ave., Maywood, IL 60153. Phone: (708) 216-3706. Fax: (708) 216-9574. E-mail: adriks{at}luc.edu.
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Journal of Bacteriology, September 1999, p. 5476-5481, Vol. 181, No. 17
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
