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Journal of Bacteriology, June 2000, p. 3274-3277, Vol. 182, No. 11
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Dual Control of sbo-alb Operon
Expression by the Spo0 and ResDE Systems of Signal Transduction under
Anaerobic Conditions in Bacillus subtilis
Michiko M.
Nakano,
Guolu
Zheng, and
Peter
Zuber*
Biochemistry and Molecular Biology, Oregon
Graduate Institute of Science and Technology, Beaverton, Oregon 97006
Received 14 December 1999/Accepted 17 March 2000
 |
ABSTRACT |
The Bacillus subtilis sbo-alb operon contains
sboA, the structural gene for the bacteriocin subtilosin,
and the alb genes required for subtilosin production.
Transcription from the sbo-alb promoter is highly induced
by oxygen limitation. The transcriptional regulation of the
sbo-alb operon is under dual control involving the
transition state regulator AbrB and the two-component regulatory proteins ResD and ResE.
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TEXT |
The production of bacteriocins is
usually induced by a combination of high cell density and low nutrient
availability (12, 13, 19). The production of antimicrobial
compounds will allow the bacterium to compete for scarce sources of
carbon, nitrogen, and energy. Bacteriocins are often produced at high
cell density to ensure that a concentration of antibiotic high enough
to have an impact on the local environment is achieved. The
spore-forming soil bacterium Bacillus subtilis produces an
assortment of antimicrobial compounds, including the antilisterial
bacteriocin subtilosin (1, 36). The structural gene for
subtilosin, sboA, resides at the 5' end of an operon that
contains the alb genes (14, 34; T. Stein,
S. Düsterhaus, A. Stroh, and K.-D. Entian, Abstr. 10th Int. Conf.
Bacilli, abstr. P103, p. 65, 1999), which are believed to function in
subtilosin chemical modification, processing, and export. The
regulation of sbo-alb operon expression is complex, since it
is induced in late growth cultures apparently in response to starvation
and is also dramatically induced by oxygen limitation (29,
34; Stein et al., Abstr. 10th Int. Conf. Bacilli). Many of
the factors governing gene expression in response to starvation (6, 8, 20, 28) and oxygen limitation (4, 25, 26, 31) have been identified in B. subtilis. Several genes
that are normally expressed in response to nutritional stress are
subject to repression by the transition state regulatory protein AbrB (29). The product of the abrB gene binds directly
to promoter DNA of the genes that are induced by starvation and
prevents their transcription during robust culture growth. We have
found that sbo-alb is one of the operons that are negatively
controlled by AbrB (34). The abrB gene is
negatively controlled by the key transcriptional regulator of
starvation-induced genes Spo0A (7, 30).
While several studies of the control of bacteriocin production in
response to high cell density and nutritional stress have been
reported, there are few that have uncovered induction of bacteriocin
synthesis in response to anaerobiosis. Colicin E1 produced by
Escherichia coli is the product of the cea gene
that is transcriptionally induced under anaerobic conditions (5, 18). Activation of cea transcription requires the FNR
protein, an iron-binding transcriptional activator of many
anaerobically induced genes (5, 18).
In this paper, we report that anaerobic induction of the
sboA-alb genes is only conditionally dependent on FNR but
absolutely requires the ResDE signal transduction complex. An
examination of the epistatic relationship of the various genes that
function in sbo-alb control shows that both the Spo0-AbrB
and ResDE systems function independently in the control of
sbo-alb transcription.
Transcription of sbo-alb is induced by oxygen
limitation.
The sbo-alb operon contains nine genes
(sboAX-albABCDEFG) and is transcribed from a
A-type promoter residing upstream of the sboA
gene (34). Although transcription proceeds through the
alb genes, there exists a sequence overlapping the end of
sboA and internal to the sboX coding sequence that can potentially form a stable hairpin-loop structure which would
be expected to impede transcription from the sbo-alb
promoter. To study the regulation of sbo-alb expression, two
lacZ transcriptional fusions were constructed as previously
described (34). One fusion, sbo
BH-lacZ,
carries a fragment of the 5' half of the sboA gene, along
with its promoter region, upstream of a promoterless lacZ gene that bears a B. subtilis ribosome-binding site. The
plasmid containing the sboBH-lacZ fusion was integrated
into an SP
specialized transducing phage. The other lacZ
fusion was constructed by inserting a fragment containing a segment of
the sbo-alb operon from the middle of albA to the
middle of albC into the integrative plasmid pMUTIN2
(33), thereby placing the fragment upstream of the
promoterless lacZ gene. Integration of this plasmid, pMUPE1
(34), into the sbo-alb operon creates an
(sbo-alb)-lacZ transcriptional fusion that does
not disrupt any of the open reading frames within the operon but does
disrupt the sbo-alb transcription unit (34).
The fusion-bearing derivatives of strain JH642 were grown aerobically
and anaerobically in 2xYT medium (23) supplemented with 1%
glucose and 0.2% KNO3 as previously described
(22). Both fusions were poorly expressed in aerobic cultures
(Fig. 1) as previously shown
(34), but a dramatic, 600-fold induction of phage-borne
sboBH-lacZ was observed in anaerobically grown cultures.
The alb::pMUPE1 fusion was also induced 40-fold
late in the growth curve under anaerobic conditions.
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FIG. 1.
Anaerobic expression of sbo-alb and
subtilosin production. Expression of sboA-lacZ and
alb-lacZ fusions in strains ORB3147
(alb::pMUPE1) and ORB3162
(SPsboBH-lacZ) under aerobic (+O2) and
anaerobic ( O2) growth conditions. -gal. act.,
-galactosidase activity.
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|
The accelerated expression of
sbo-alb in anaerobically grown
cells prompted us to determine if transcription from the
sbo-alb promoter is stimulated under oxygen limitation and
if the same
promoter is utilized in anaerobic growth as in aerobic
growth.
Total RNA was purified, as described in a previous report
(
24),
from JH642 cells collected at
T2 of the growth curve (2 h after
the end of
exponential phase). Cultures were grown aerobically
and anaerobically
at 37°C in 2 × YT medium supplemented with 1%
glucose and
0.2% KNO
3. Primer extension was performed as previously
described using oligonucleotide osboP4 (
34). An at least
10-fold
greater amount of primer extension product was produced in
reaction
mixtures containing RNA from anaerobically grown cells (Fig.
2A,
lane 6) than in reaction mixtures
containing RNA from aerobically
grown cells (lane 5). It was also
observed that the same transcriptional
start site was utilized under
both aerobic and anaerobic conditions.
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FIG. 2.
(A) Utilization of the same transcription start site in
the sbo-alb promoter region under aerobic and anaerobic
conditions. Tenfold less primer extension reaction mixture was applied
to lane 6 (RNA from anaerobic cultures) than was applied to lane 5 (RNA
from aerobic cultures). Sequencing reactions G, A, T, and C are in
lanes 1, 2, 3, and 4, respectively. (B) Nucleotide sequence of the
sbo-alb promoter region and similarity to the regulatory
region of the resA operon. The ATG start site of the
sboA gene and its ribosome-binding site (SD) are shown. The
10 and 35 regions are indicated, as is the transcription start site
(*), and a region of approximate dyad symmetry upstream of the 35
sequence is marked with arrows beneath the nucleotide sequence. A
broken bar above the nucleotide sequence extending from 36 to 62
marks the sequence identity between the resA and
sbo-alb regulatory regions. The sequence above the bar
indicates the nucleotide residues of the corresponding region in the
resA promoter region.
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|
Anaerobic induction of sbo-alb requires the ResDE
signal transduction system.
The involvement of the known
regulators of anaerobic gene control was next examined by measuring the
expression of sboBH-lacZ in resDE (26,
31), fnr (4, 26), and narGH
(21) mutant cells. The narGHJ genes encode
subunits of respiratory nitrate reductase (9, 15) and are
required for the expression of some anaerobically induced genes in the
absence of nitrite (15, 26). These genes also require
fnr, since narGHJI transcription is activated by
the FNR protein (15, 22, 26). As shown in Table
1, all three mutations abolish
sboBH-lacZ expression in 2xYT-glucose-nitrate-grown cells
under anaerobic conditions. If nitrite (10 mM KNO2) is
substituted for nitrate, then expression of sboBH-lacZ no
longer requires fnr and narGH but still is
absolutely dependent on the ResDE system (Table 1).
Transcription of sbo-alb is controlled by two
independent regulatory pathways.
The transition state regulator
AbrB exerts negative control over transcription from the
sbo-alb promoter (34). This form of regulation
was reexamined in anaerobically grown cells bearing the
sboBH-lacZ fusion. A mutation in the
spo0A gene (10) which results in overproduction
of the abrB product causes a sharp reduction in
sboBH-lacZ expression in cells grown anaerobically (Table 1). The effect of a spo0A mutation is overcome by
introducing a mutation in abrB (34) (strain
ORB3438, Table 1). Since the temporal regulation of sbo-alb
expression is still observed in the abrB and spo0A
abrB mutants (data not shown), ResD might be activated only after
exponential growth, probably as a result of nitrite accumulation.
However, we cannot rule out the possibility that another regulator is
involved in the postexponential induction of sboA-alb.
ResDE, like the Spo0 system, could positively regulate
sbo-alb transcription by repressing the
abrB gene
or indirectly affect
AbrB concentration and/or activity. If this were
the case, then
we would expect an
abrB null mutation to
result in
sbo-alb expression
in the absence of ResDE.
Examination of
sboBH-lacZ expression
in the
resDE
abrB double mutant showed that the ResDE system is
still required
for
sbo-alb transcription in the absence of AbrB
protein
(Table
1).
To further investigate the relationship among Spo0A, AbrB, and ResDE,
the expression of ResDE-controlled genes was examined
in
spo0A,
abrB, and
spo0A abrB mutant
cells bearing either an
fnr (
26)-, an
hmp (flavohemoglobin) (
15)-, or an
nasD (nitrite
reductase) (
22)-
lacZ
construct, each of which requires ResDE
for expression. If expression
of
resDE or the activity of their
products required
spo0A or was repressed by AbrB, then a
spo0A mutation would have resulted in reduced expression of the
resDE-controlled
lacZ fusions. No effect of a
spo0A or an
abrB mutation on
lacZ expression was detected (data not shown), indicating that Spo0A
and
AbrB do not influence the activity of ResDE in anaerobically
grown
cells. The addition of nitrite, which is thought to be necessary
for
ResDE-dependent activation of anaerobically induced genes,
did not
significantly overcome the inhibition of
sbo-alb
transcription
caused by AbrB overproduction in a
spo0A
mutant background (Table
1). These results show that the Spo0-AbrB and
ResDE systems of
control operate independently of each other. An
earlier observation
that membrane-bound nitrate reductase was
hyperactive in Spo0
mutants (
3) was explained by possible
membrane alteration in
the mutant strains; however, an alternative
possibility that AbrB
is a positive regulator of the
narGHJI
operon is worth
examining.
The results presented herein and those from previously published
studies (
34) provide compelling evidence that Spo0-AbrB-
and
ResDE-dependent mechanisms of control are exerted at the level
of
sbo-alb transcription initiation. Inspection of the
sbo-alb regulatory region reveals a sequence extending from
37 to
62
that contains a region of approximate dyad symmetry and
sequences
identical to the
37 to
62 sequence within the regulatory
region
of the
resA operon which is also controlled by ResDE
(Fig.
2B)
(
2,
31). Access to the
sbo-alb promoter
region may be blocked
by the AbrB protein early in the growth curve.
Following Spo0A
repression of
abrB when cells approach
stationary phase, ResD,
activated as nitrite accumulates in the cell,
will gain access
to the region upstream of the promoter
35 sequence,
where it
will interact with RNA polymerase to stimulate transcription
initiation.
Under aerobic growth conditions, Spo0A-P will accumulate as cultures
approach stationary phase due to the activities of KinA,
-B, -C, and
-D, all of which are histidine protein kinases that
donate high-energy
phosphate to the Spo0 phosphorelay (
6,
7,
11,
16,
17,
27,
32). The initial phosphorylation of
Spo0A is thought to depend on
KinC (
16,
17). This results
in a level of Spo0A-P sufficient
for repression of the
abrB gene.
KinC has been shown to
phosphorylate Spo0A in the absence of other
Spo0 phosphorelay
components, but its preferred target is believed
to be Spo0F (
11,
17). It seems that the KinC-Spo0 system is
functional in
anaerobically grown
B. subtilis cells in which
sbo-alb expression is induced. However,
B. subtilis cells do not readily
undergo sporulation late in the
growth curve when grown anaerobically
in sporulation medium (data not
shown;
9). It is not known
if the other kinases that
supply the Spo0 phosphorelay with high-energy
phosphate are functional
in anaerobically grown
cells.
Although
sbo-alb undergoes significant transcriptional
induction when cells encounter anaerobic conditions, this is not
accompanied
by a proportional increase in antilisterial activity, at
least
not under the growth conditions used in this study (data not
shown).
However, an increase in the anaerobic production of subtilosin
has been reported (Stein et al., 10th Int. Conf. Bacilli). Mutations
in
sboA or in any of the
alb genes do not
significantly impair
anaerobic growth (data not shown). It is not
obvious why the cell
would benefit from the massive increase in
sbo-alb expression
during anaerobiosis. It is possible that
we have not used the
appropriate anaerobic growth conditions required
for active subtilosin
production. It is also possible that the cell
accumulates inactive
precursors of subtilosin, which then undergo
oxygen-dependent
modifications to yield an active peptide when an
aerobic environment
is encountered. A greater knowledge of
sbo-alb gene products and
their function, as well as an
examination of other antimicrobial
production systems in anaerobically
grown
Bacillus species, may
provide clues as to the role
bacteriocins play in the anaerobic
life of
bacteria.
| |
ACKNOWLEDGMENTS |
Support for this work was provided by grant GM45898 from the
National Institutes of Health (to P.Z.), grant MCB-9996014 from the
National Science Foundation (to M.M.N.), and a grant from The Oregon
Research Foundation. P.Z. gratefully acknowledges support from E. I. du Pont de Nemours, Inc.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Biochemistry and Molecular Biology, Oregon Graduate Institute of
Science and Technology, 20000 NW Walker Rd., Beaverton, OR 97006. Phone: (503) 748-7335. Fax: (503) 748-1464. E-mail:
pzuber{at}bmb.ogi.edu.
| |
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Journal of Bacteriology, June 2000, p. 3274-3277, Vol. 182, No. 11
0021-9193/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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